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Intestinal anti-inflammatory activity of Sasa quelpaertensis leaf extract by suppressing lipopolysaccharide-stimulated inflammatory mediators in intestinal epithelial Caco-2 cells co-cultured with RAW 264.7 macrophage cells

  • Kim, Kyung-Mi (Department of Nutritional Science and Food Management, Ewha Womans University) ;
  • Kim, Yoo-Sun (Department of Nutritional Science and Food Management, Ewha Womans University) ;
  • Lim, Ji Ye (Department of Nutritional Science and Food Management, Ewha Womans University) ;
  • Min, Soo Jin (Department of Nutritional Science and Food Management, Ewha Womans University) ;
  • Ko, Hee-Chul (Jeju Sasa Industry Development Agency, Jeju National University) ;
  • Kim, Se-Jae (Department of Biology, Jeju National University) ;
  • Kim, Yuri (Department of Nutritional Science and Food Management, Ewha Womans University)
  • Received : 2014.04.03
  • Accepted : 2014.07.02
  • Published : 2015.02.01

Abstract

BACKGROUND/OBJECTIVES: Inflammatory bowel disease (IBD), including Crohn's disease and ulcerative colitis, involves chronic inflammation of the gastrointestinal tract. Previously, Sasa quelpaertensis leaves have been shown to mediate anti-inflammation and anti-cancer effects, although it remains unclear whether Sasa leaves are able to attenuate inflammation-related intestinal diseases. Therefore, the aim of this study was to investigate the anti-inflammatory effects of Sasa quelpaertensis leaf extract (SQE) using an in vitro co-culture model of the intestinal epithelial environment. MATERIALS/METHODS: An in vitro co-culture system was established that consisted of intestinal epithelial Caco-2 cells and RAW 264.7 macrophages. Treatment with lipopolysaccharide (LPS) was used to induce inflammation. RESULTS: Treatment with SQE significantly suppressed the secretion of LPS-induced nitric oxide (NO), prostaglandin $E_2$ ($PGE_2$), IL-6, and IL-$1{\beta}$ in co-cultured RAW 264.7 macrophages. In addition, expressions of inducible nitric oxide synthase (iNOS), cyclooxygenase (COX)-2, and tumor necrosis factor (TNF)-${\alpha}$ were down-regulated in response to inhibition of $I{\kappa}B{\alpha}$ phosphorylation by SQE. Compared with two bioactive compounds that have previously been identified in SQE, tricin and P-coumaric acid, SQE exhibited the most effective anti-inflammatory properties. CONCLUSIONS: SQE exhibited intestinal anti-inflammatory activity by inhibiting various inflammatory mediators mediated through nuclear transcription factor kappa-B (NF-kB) activation. Thus, SQE has the potential to ameliorate inflammation-related diseases, including IBD, by limiting excessive production of pro-inflammatory mediators.

Acknowledgement

Grant : Cooperative Research Program for Agriculture Science & Technology Development

Supported by : Rural Development Administration

References

  1. Arai F, Takahashi T, Furukawa K, Matsushima K, Asakura H. Mucosal expression of interleukin-6 and interleukin-8 messenger RNA in ulcerative colitis and in Crohn's disease. Dig Dis Sci 1998;43:2071-9. https://doi.org/10.1023/A:1018815432504
  2. Chung HL, Yue GG, To KF, Su YL, Huang Y, Ko WH. Effect of Scutellariae Radix extract on experimental dextran-sulfate sodiuminduced sodiuminduced colitis in rats. World J Gastroenterol 2007;13:5605-11. https://doi.org/10.3748/wjg.v13.i42.5605
  3. Loftus EV Jr, Sandborn WJ. Epidemiology of inflammatory bowel disease. Gastroenterol Clin North Am 2002;31:1-20. https://doi.org/10.1016/S0889-8553(01)00002-4
  4. Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol 2003;3:521-33. https://doi.org/10.1038/nri1132
  5. Menditto A, Menotti A, Morisi G, Patriarca M, Spagnolo A. Serum ascorbic acid levels in men aged 55-75 years: association to selected social factors and biochemical parameters. Arch Gerontol Geriatr 1992;15 Suppl 1:257-65. https://doi.org/10.1016/S0167-4943(05)80025-1
  6. Nishitani Y, Tanoue T, Yamada K, Ishida T, Yoshida M, Azuma T, Mizuno M. Lactococcus lactis subsp. cremoris FC alleviates symptoms of colitis induced by dextran sulfate sodium in mice. Int Immunopharmacol 2009;9:1444-51. https://doi.org/10.1016/j.intimp.2009.08.018
  7. Bode H, Schmitz H, Fromm M, Scholz P, Riecken EO, Schulzke JD. IL-1beta and TNF-alpha, but not IFN-alpha, IFN-gamma, IL-6 or IL-8, are secretory mediators in human distal colon. Cytokine 1998;10: 457-65. https://doi.org/10.1006/cyto.1997.0307
  8. Brozek W, Bises G, Fabjani G, Cross HS, Peterlik M. Clone-specific expression, transcriptional regulation, and action of interleukin-6 in human colon carcinoma cells. BMC Cancer 2008;8:13. https://doi.org/10.1186/1471-2407-8-13
  9. Edwards MR, Bartlett NW, Clarke D, Birrell M, Belvisi M, Johnston SL. Targeting the NF-kappaB pathway in asthma and chronic obstructive pulmonary disease. Pharmacol Ther 2009;121:1-13. https://doi.org/10.1016/j.pharmthera.2008.09.003
  10. Wong ET, Tergaonkar V. Roles of NF-kappaB in health and disease: mechanisms and therapeutic potential. Clin Sci (Lond) 2009;116: 451-65. https://doi.org/10.1042/CS20080502
  11. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990;98: 694-702. https://doi.org/10.1016/0016-5085(90)90290-H
  12. Sadlack B, Merz H, Schorle H, Schimpl A, Feller AC, Horak I. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell 1993;75:253-61. https://doi.org/10.1016/0092-8674(93)80067-O
  13. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993;75:263-74. https://doi.org/10.1016/0092-8674(93)80068-P
  14. Ohta N, Hiroi T, Kweon MN, Kinoshita N, Jang MH, Mashimo T, Miyazaki J, Kiyono H. IL-15-dependent activation-induced cell death-resistant Th1 type CD8 alpha beta + NK1.1 + T cells for the development of small intestinal inflammation. J Immunol 2002;169: 460-8. https://doi.org/10.4049/jimmunol.169.1.460
  15. Farombi EO, Adedara IA, Ajayi BO, Ayepola OR, Egbeme EE. Kolaviron, a natural antioxidant and anti-inflammatory phytochemical prevents dextran sulphate sodium-induced colitis in rats. Basic Clin Pharmacol Toxicol 2013;113:49-55.
  16. Okabe S, Takeuchi K, Takagi K, Shibata M. Stimulatory effect of the water extract of bamboo grass (Folin solution) on gastric acid secretion in pylorus-ligated rats. Jpn J Pharmacol 1975;25:608-9. https://doi.org/10.1254/jjp.25.608
  17. Choi YJ, Lim HS, Choi JS, Shin SY, Bae JY, Kang SW, Kang IJ, Kang YH. Blockade of chronic high glucose-induced endothelial apoptosis by Sasa borealis bamboo extract. Exp Biol Med (Maywood) 2008; 233:580-91. https://doi.org/10.3181/0707-RM-205
  18. Ren M, Reilly RT, Sacchi N. Sasa health exerts a protective effect on Her2/NeuN mammary tumorigenesis. Anticancer Res 2004;24: 2879-84.
  19. Kang SI, Shin HS, Kim HM, Hong YS, Yoon SA, Kang SW, Kim JH, Ko HC, Kim SJ. Anti-obesity properties of a Sasa quelpaertensis extract in high-fat diet-induced obese mice. Biosci Biotechnol Biochem 2012;76:755-61. https://doi.org/10.1271/bbb.110868
  20. Kim K, Lim JY, Min S, Lim Y, Ko H, Kim S, Kim Y. Sasa quelpaertensis leaf extract suppresses dextran sulfate sodium (DSS)-induced colitis im mice. Nutr Res. Forthcoming 2014.
  21. Tanoue T, Nishitani Y, Kanazawa K, Hashimoto T, Mizuno M. In vitro model to estimate gut inflammation using co-cultured Caco-2 and RAW264.7 cells. Biochem Biophys Res Commun 2008;374:565-9. https://doi.org/10.1016/j.bbrc.2008.07.063
  22. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem 1976;72:248-54. https://doi.org/10.1016/0003-2697(76)90527-3
  23. Wilson KT, Ramanujam KS, Mobley HL, Musselman RF, James SP, Meltzer SJ. Helicobacter pylori stimulates inducible nitric oxide synthase expression and activity in a murine macrophage cell line. Gastroenterology 1996;111:1524-33. https://doi.org/10.1016/S0016-5085(96)70014-8
  24. Choi EM, Hwang JK. Effects of Morus alba leaf extract on the production of nitric oxide, prostaglandin E2 and cytokines in RAW264.7 macrophages. Fitoterapia 2005;76:608-13. https://doi.org/10.1016/j.fitote.2005.05.006
  25. Shapira L, Soskolne WA, Houri Y, Barak V, Halabi A, Stabholz A. Protection against endotoxic shock and lipopolysaccharide-induced local inflammation by tetracycline: correlation with inhibition of cytokine secretion. Infect Immun 1996;64:825-8.
  26. Jeoung BR, Lee KD, Na CS, Kim YE, Kim B, Kim YR. Ganghwaljetongyeum, an anti-arthritic remedy, attenuates synoviocyte proliferation and reduces the production of proinflammatory mediators in macrophages: the therapeutic effect of GHJTY on rheumatoid arthritis. BMC Complement Altern Med 2013;13:47. https://doi.org/10.1186/1472-6882-13-47
  27. Lee H, Bae S, Choi BW, Yoon Y. WNT/beta-catenin pathway is modulated in asthma patients and LPS-stimulated RAW264.7 macrophage cell line. Immunopharmacol Immunotoxicol 2012;34: 56-65. https://doi.org/10.3109/08923973.2011.574704
  28. Okada Y, Tsuzuki Y, Narimatsu K, Sato H, Ueda T, Hozumi H, Sato S, Hokari R, Kurihara C, Komoto S, Watanabe C, Tomita K, Kawaguchi A, Nagao S, Miura S. 1,4-Dihydroxy-2-naphthoic acid from Propionibacterium freudenreichii reduces inflammation in interleukin-10-deficient mice with colitis by suppressing macrophage-derived proinflammatory cytokines. J Leukoc Biol 2013;94:473-80. https://doi.org/10.1189/jlb.0212104
  29. MacDermott RP. Chemokines in the inflammatory bowel diseases. J Clin Immunol 1999;19:266-72. https://doi.org/10.1023/A:1020583306627
  30. Ogata H, Hibi T. Cytokine and anti-cytokine therapies for inflammatory bowel disease. Curr Pharm Des 2003;9:1107-13. https://doi.org/10.2174/1381612033455035
  31. Feagan BG, Reinisch W, Rutgeerts P, Sandborn WJ, Yan S, Eisenberg D, Bala M, Johanns J, Olson A, Hanauer SB. The effects of infliximab therapy on health-related quality of life in ulcerative colitis patients. Am J Gastroenterol 2007;102:794-802. https://doi.org/10.1111/j.1572-0241.2007.01094.x
  32. Pettus BJ, Bielawski J, Porcelli AM, Reames DL, Johnson KR, Morrow J, Chalfant CE, Obeid LM, Hannun YA. The sphingosine kinase 1/sphingosine-1-phosphate pathway mediates COX-2 induction and PGE2 production in response to TNF-alpha. FASEB J 2003;17: 1411-21. https://doi.org/10.1096/fj.02-1038com
  33. Appleby SB, Ristimaki A, Neilson K, Narko K, Hla T. Structure of the human cyclo-oxygenase-2 gene. Biochem J 1994;302 (Pt 3):723-7. https://doi.org/10.1042/bj3020723
  34. Beg AA, Finco TS, Nantermet PV, Baldwin AS Jr. Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of I kappa B alpha: a mechanism for NF-kappa B activation. Mol Cell Biol 1993;13:3301-10. https://doi.org/10.1128/MCB.13.6.3301
  35. Park OJ, Surh YJ. Chemopreventive potential of epigallocatechin gallate and genistein: evidence from epidemiological and laboratory studies. Toxicol Lett 2004;150:43-56. https://doi.org/10.1016/j.toxlet.2003.06.001
  36. Bai SK, Lee SJ, Na HJ, Ha KS, Han JA, Lee H, Kwon YG, Chung CK, Kim YM. beta-Carotene inhibits inflammatory gene expression in lipopolysaccharide-stimulated macrophages by suppressing redoxbased NF-kappaB activation. Exp Mol Med 2005;37:323-34. https://doi.org/10.1038/emm.2005.42
  37. Liu H, Sidiropoulos P, Song G, Pagliari LJ, Birrer MJ, Stein B, Anrather J, Pope RM. TNF-alpha gene expression in macrophages: regulation by NF-kappa B is independent of c-Jun or C/EBP beta. J Immunol 2000;164:4277-85. https://doi.org/10.4049/jimmunol.164.8.4277
  38. Rosillo MA, Sanchez-Hidalgo M, Cardeno A, de la Lastra CA. Protective effect of ellagic acid, a natural polyphenolic compound, in a murine model of Crohn's disease. Biochem Pharmacol 2011; 82:737-45. https://doi.org/10.1016/j.bcp.2011.06.043
  39. Chu X, Ci X, He J, Jiang L, Wei M, Cao Q, Guan M, Xie X, Deng X, He J. Effects of a natural prolyl oligopeptidase inhibitor, rosmarinic acid, on lipopolysaccharide-induced acute lung injury in mice. Molecules 2012;17:3586-98. https://doi.org/10.3390/molecules17033586
  40. Otani K, Yanaura S, Yuda Y, Kawaoto H, Kajita T, Hirano F, Osawa F, Inouye S. Histo-chemical studies on the anti-ulcer effect of bamboo grass in rats. Int J Tissue React 1990;12:319-32.
  41. Moon JY, Yang EJ, Kim SS, Kang JY, Kim GO, Lee NH, Hyun CG. Sasa quelpaertensis phenylpropanoid derivative suppresses lipopolysaccharide-induced nitric oxide synthase and cyclo-oxygenase-2 expressions in RAW 264.7 cells. Yakugaku Zasshi 2011;131:961-7. https://doi.org/10.1248/yakushi.131.961
  42. Zang LY, Cosma G, Gardner H, Shi X, Castranova V, Vallyathan V. Effect of antioxidant protection by P-coumaric acid on low-density lipoprotein cholesterol oxidation. Am J Physiol Cell Physiol 2000;279:C954-60. https://doi.org/10.1152/ajpcell.2000.279.4.C954
  43. Pragasam SJ, Venkatesan V, Rasool M. Immunomodulatory and anti-inflammatory effect of P-coumaric acid, a common dietary polyphenol on experimental inflammation in rats. Inflammation 2013;36:169-76. https://doi.org/10.1007/s10753-012-9532-8
  44. Perez-Alvarez V, Bobadilla RA, Muriel P. Structure-hepatoprotective activity relationship of 3,4-dihydroxycinnamic acid (caffeic acid) derivatives. J Appl Toxicol 2001;21:527-31. https://doi.org/10.1002/jat.806
  45. Shalini V, Bhaskar S, Kumar KS, Mohanlal S, Jayalekshmy A, Helen A. Molecular mechanisms of anti-inflammatory action of the flavonoid, tricin from Njavara rice (Oryza sativa L.) in human peripheral blood mononuclear cells: possible role in the inflammatory signaling. Int Immunopharmacol 2012;14:32-8. https://doi.org/10.1016/j.intimp.2012.06.005
  46. Liu RH. Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals. Am J Clin Nutr 2003;78:517S-520S. https://doi.org/10.1093/ajcn/78.3.517S

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