DOI QR코드

DOI QR Code

Antioxidant effect and inhibitory activities of ethyl acetate fraction from Gardenia jasminoides extract on nitric oxide production and pancreatic cancer cell proliferation

치자 에틸아세테이트 분획의 산화방지, 산화질소 제거 및 암세포증식 억제 활성

  • Received : 2017.11.16
  • Accepted : 2018.01.11
  • Published : 2018.04.30

Abstract

To evaluate the radical scavenging activity of phenolic-rich fractions of Gardenia jasminoides, we first measured the levels of total polyphenols in hexane, ethyl acetate, and butanol fractions from the extract of G. jasminoides. The ethyl acetate fraction of G. jasminoides extract (GJ-EA) showed high level of phenolics, potent reducing power, and 2,2-diphenyl-1-picrylhydrazyl/2,2'-azino-bis 3-ethylbenzothiazoline-6-sulfonic acid radical scavenging effect. In addition, GJ-EA inhibited the overproduction of nitric oxide in lipopolysaccharide-activated BV-2 microglia. Furthermore, we found that GJ-EA suppressed $H_2O_2$-induced PANC-1 pancreatic cancer cell proliferation in a concentration-dependent manner and also reduced their migratory ability. These results suggest that GJ-EA may be a good source for functional foods with antioxidant and chemo-preventive activities.

Keywords

Gardenia jasminoides;antioxidant activity;radical scavenging;pancreatic cancer;tumor-migration

References

  1. Almasalmeh A, Krenc D, Wu B, Beitz E. Structural determinants of the hydrogen peroxide permeability of aquaporins. FEBS J. 281: 647-656 (2014) https://doi.org/10.1111/febs.12653
  2. Cao L, Liu J, Zhang L, Xiao X, Li W. Curcumin inhibits $H_2O_2$- induced invasion and migration of human pancreatic cancer via suppression of the ERK/NF-${\kappa}B$ pathway. Oncol. Rep. 36: 2245- 2251 (2016) https://doi.org/10.3892/or.2016.5044
  3. Carey GB, Roy SK, Daino H. The natural tumorcide Manumycin-A targets protein phosphatase $1{\alpha}$ and reduces hydrogen peroxide to induce lymphoma apoptosis. Exp. Cell Res. 332: 136-145 (2015) https://doi.org/10.1016/j.yexcr.2014.12.009
  4. Castaneda OA, Lee SC, Ho CT, Huang TC. Macrophages in oxidative stress and models to evaluate the antioxidant function of dietary natural compounds. J. Food Drug Anal. 25: 111-118 (2017) https://doi.org/10.1016/j.jfda.2016.11.006
  5. Chang WL, Wang HY, Shi LS, Lai JH, Lin HC. Immunosuppressive iridoids from the fruits of Gardenia jasminoides. J. Nat. Prod. 68: 1683-1685 (2005) https://doi.org/10.1021/np0580816
  6. Chen Y, Cai L, Zhao C, Xu HC, Cao CY, Liu Y, Jia L, Yin HX, Chen C, Zhang H. Spectroscopic, stability and radical-scavenging properties of a novel pigment from gardenia. Food Chem. 109: 269-277 (2008a) https://doi.org/10.1016/j.foodchem.2007.10.023
  7. Chen S, Sun P, Zhao X, Yi R, Qian J, Shi Y, Wang R. Gardenia jasminoides has therapeutic effects on L-NNA-induced hypertension in vivo. Mol. Med. Rep. 15: 4360-4373 (2017) https://doi.org/10.3892/mmr.2017.6542
  8. Chen Y, Zhang H, Li YX, Cai L, Huang J, Zhao C, Jia L, Buchanan R, Yang T, Jiang LJ. Crocin and geniposide profiles and radical scavenging activity of gardenia fruits (Gardenia jasminoides Ellis) from different cultivars and at the various stages of maturation. Fitoterapia 81: 269-273 (2010) https://doi.org/10.1016/j.fitote.2009.09.011
  9. Chen Y, Zhang H, Tian X, Zhao C, Cai L, Liu Y, Jia L, Yin HX, Chen C. Antioxidant potential of crocins and ethanol extracts of Gardenia jasminoides ELLIS and Crocus sativus L.: A relationship investigation between antioxidant activity and crocin contents. Food Chem. 109: 484-492 (2008b) https://doi.org/10.1016/j.foodchem.2007.09.080
  10. Danta CC, Piplani P. The discovery and development of new potential antioxidant agents for the treatment of neurodegenerative diseases. Expert Opin. Drug Dis. 9: 1205-1222 (2014) https://doi.org/10.1517/17460441.2014.942218
  11. Debnath T, Park PJ, Debnath NC, Samad NB, Park HW, Lim BO. Antioxidant activity of Gardenia jasminoides Ellis fruit extrcts. Food Chem. 128: 697-703 (2011) https://doi.org/10.1016/j.foodchem.2011.03.090
  12. Fu Y, Liu B, Liu J, Liu Z, Liang D, Li F, Li D, Cao Y, Zhang X, Zhang N, Yang Z. Geniposide, from Gardenia jasminoides Ellis, inhibits the inflammatory response in the primary mouse macrophages and mouse models. Int. Immunopharmacol. 14: 792-798 (2012) https://doi.org/10.1016/j.intimp.2012.07.006
  13. Gedik S, Erdemli ME, Gul M, Yigitcan B, Gozukara Bag H, Aksungur Z, Altinoz E. Hepatoprotective effects of crocin on biochemical and histopathological alterations following acrylamide-induced liver injury in Wistar rats. Biomed. Pharmacother. 95: 764-770 (2017) https://doi.org/10.1016/j.biopha.2017.08.139
  14. Gupta RK, Patel AK, Shah N, Chaudhary AK, Jha UK, Yadav UC, Gupta PK, Pakuwal U. Oxidative stress and antioxidants in disease and cancer: A review. Asian Pac. J. Cancer P. 15: 4405- 4409 (2014) https://doi.org/10.7314/APJCP.2014.15.11.4405
  15. Hara-Chikuma M, Watanabe S, Satooka H. Involvement of aquaporin- 3 in epidermal growth factor receptor signaling via hydrogen peroxide transport in cancer cells. Biochem. Bioph. Res. Co. 471: 603-609 (2016) https://doi.org/10.1016/j.bbrc.2016.02.010
  16. Islam MT. Oxidative stress and mitochondrial dysfunction-linked neurodegenerative disorders. Neurol. Res. 39: 73-82 (2017) https://doi.org/10.1080/01616412.2016.1251711
  17. Jasprica I, Bojic M, Mornar A, Besic E, Bucan K, Medic-Saric M. Evaluation of antioxidative activity of Croatian propolis samples using DPPH* and ABTS*+ stable free radical assays. Molecules 12: 1006-1021 (2007) https://doi.org/10.3390/12051006
  18. Ju J, Kwak Y, Hao X, Yang CS. Inhibitory effects of calcium against intestinal cancer in human colon cancer cells and Apc(Min/+) mice. Nutr. Res. Pract. 6: 396-404 (2012) https://doi.org/10.4162/nrp.2012.6.5.396
  19. Kim ES, Jeong CS, Moon A. Genipin, a constituent of Gardenia jasminoides Ellis, induces apoptosis and inhibits invasion in MDAMB- 231 breast cancer cells. Oncol. Rep. 27: 567-572 (2012)
  20. Kim SJ, Kim JK, Lee DU, Kwak JH, Lee SM. Genipin protects lipopolysaccharide-induced apoptotic liver damage in D-galactosamine- sensitized mice. Eur. J. Pharmacol. 635: 188-193 (2010) https://doi.org/10.1016/j.ejphar.2010.03.007
  21. Kim HJ, Kim EJ, Seo SH, Shin CG, Jin C, Lee YS. Vanillic acid glycoside and quinic acid derivatives from Gardeniae Fructus. J. Nat. Prod. 69: 600-603 (2006) https://doi.org/10.1021/np050447r
  22. Kundu S, Ghosh P, Datta S, Ghosh A, Chattopadhyay S, Chatterjee M. Oxidative stress as a potential biomarker for determining disease activity in patients with rheumatoid arthritis. Free Radical Res. 46: 1482-1489 (2012) https://doi.org/10.3109/10715762.2012.727991
  23. Lee CT, Yu LE, Wang JY. Nitroxide antioxidant as a potential strategy to attenuate the oxidative/nitrosative stress induced by hydrogen peroxide plus nitric oxide in cultured neurons. Nitric Oxide 54: 38-50 (2016) https://doi.org/10.1016/j.niox.2016.02.001
  24. Lim W, Kim O, Jung J, Ko Y, Ha J, Oh H, Lim H, Kwon H, Kim I, Kim J, Kim M, Kim S, Kim BK, Kim S, Kang BC, Choi H, Kim O. Dichloromethane fraction from Gardenia jasminoides: DNA topoisomerase 1 inhibition and oral cancer cell death induction. Pharm. Biol. 48: 1354-1360 (2010) https://doi.org/10.3109/13880209.2010.483246
  25. Liu H, Chen YF, Li F, Zhang HY. Fructus Gardenia (Gardenia jasminoides J. Ellis) phytochemistry, pharmacology of cardiovascular, and safety with the perspective of new drugs development. J. Asian Nat. Prod. Res. 15: 94-110 (2013) https://doi.org/10.1080/10286020.2012.723203
  26. Liu H, Liu X, Zhang C, Zhu H, Xu Q, Bu Y, Lei Y. Redox imbalance in the development of colorectal cancer. J. Cancer. 8: 1586- 1597 (2017) https://doi.org/10.7150/jca.18735
  27. Losada-Barreiro S, Bravo-Diaz C. Free radicals and polyphenols: The redox chemistry of neurodegenerative diseases. Eur. J. Med. Chem. 133: 379-402 (2017) https://doi.org/10.1016/j.ejmech.2017.03.061
  28. Manach C, Williamson G, Morand C, Scalbert A, Remesy C. Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am. J. Clin. Nutr. 81: 230S-242S (2005) https://doi.org/10.1093/ajcn/81.1.230S
  29. Oliveira H, Cai X, Zhang Q, de Freitas V, Mateus N, He J, Fernandes I. Gastrointestinal absorption, antiproliferative and antiinflammatory effect of the major carotenoids of Gardenia jasminoides Ellis on cancer cells. Food Funct. 8: 1672-1679 (2017) https://doi.org/10.1039/C7FO00091J
  30. Padda MS, Picha DH. Methodology optimization for quantification of total phenolics and individual phenolic acids in sweet potato (Ipomoea batatas L.) roots. J. Food Sci. 72: C412-C416 (2007) https://doi.org/10.1111/j.1750-3841.2007.00448.x
  31. Peng K, Yang L, Zhao S, Chen L, Zhao F, Qiu F. Chemical constituents from the fruit of Gardenia jasminoides and their inhibitory effects on nitric oxide production. Bioorg. Med. Chem. Lett. 23: 1127-1131 (2013) https://doi.org/10.1016/j.bmcl.2012.11.099
  32. Poprac P, Jomova K, Simunkova M, Kollar V, Rhodes CJ, Valko M. Targeting free radicals in oxidative stress-related human diseases. Trends Pharmacol. Sci. 38: 592-607 (2017) https://doi.org/10.1016/j.tips.2017.04.005
  33. Quideau S, Deffieux D, Douat-Casassus C, Pouysegu L. Plant polyphenols: chemical properties, biological activities, and synthesis. Angew. Chem. Int. Edit. 50: 586-621 (2011) https://doi.org/10.1002/anie.201000044
  34. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Bio. Med. 26: 1231-1237 (1999) https://doi.org/10.1016/S0891-5849(98)00315-3
  35. Scheel C, Weinberg RA. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links. Semin. Cancer Biol. 22: 396-403 (2012) https://doi.org/10.1016/j.semcancer.2012.04.001
  36. Shon DH, Choi DW, Kim MH. Improvement of anti-inflammation activity of Gardenia fructus extract by the treatment of ${\beta}$-glucosidase. Korean J. Food Sci. Technol. 44: 331-336 (2012) https://doi.org/10.9721/KJFST.2012.44.3.331
  37. Suzuki Y, Kondo K, Ikeda Y, Umemura K. Antithrombotic effect of geniposide and genipin in the mouse thrombosis model. Planta Med. 67: 807-810 (2001) https://doi.org/10.1055/s-2001-18842
  38. Wang Y, Chen Y, Deng L, Cai S, Liu J, Li W, Du L, Cui G, Xu X, Lu T, Chen P, Zhang H. Systematic separation and purification of iridoid glycosides and crocetin derivatives from Gardenia jasminoides Ellis by high-speed counter-current chromatography. Phytochem. Analysis 26: 202-208 (2015) https://doi.org/10.1002/pca.2553
  39. Wang L, Liu S, Zhang X, Xing J, Liu Z, Song F. A strategy for identification and structural characterization of compounds from Gardenia jasminoides by integrating macroporous resin column chromatography and liquid chromatography-tandem mass spectrometry combined with ion-mobility spectrometry. J. Chromatogr. A. 1452: 47-57 (2016) https://doi.org/10.1016/j.chroma.2016.05.026
  40. Wang Q, Shen W, Tao GQ, Sun J, Shi LP. Study on the proliferation of human gastric cancer cell AGS by activation of EGFR in $H_2O_2$. Eur. Rev. Med. Pharmaco. 21: 1006-1012 (2017)
  41. Watanabe T, Terabe S. Analysis of natural food pigments by capillary electrophoresis. J. Chromatogr. A. 880: 311-322 (2000) https://doi.org/10.1016/S0021-9673(00)00209-0
  42. Wu SY, Wang GF, Liu ZQ, Rao JJ, Lu L, Xu W, Wu SG, Zhang JJ. Effect of geniposide, a hypoglycemic glucoside, on hepatic regulating enzymes in diabetic mice induced by a high-fat diet and streptozotocin. Acta Pharmacol. Sin. 30: 202-208 (2009) https://doi.org/10.1038/aps.2008.17
  43. Xiao W, Li S, Wang S, Ho CT. Chemistry and bioactivity of Gardenia jasminoides. J. Food Drug Anal. 25: 43-61 (2017) https://doi.org/10.1016/j.jfda.2016.11.005
  44. Xu B, Li YL, Xu M, Yu CC, Lian MQ, Tang ZY, Li CX, Lin Y. Geniposide ameliorates TNBS-induced experimental colitis in rats via reducing inflammatory cytokine release and restoring impaired intestinal barrier function. Acta Pharmacol. Sin. 38: 688-698 (2017) https://doi.org/10.1038/aps.2016.168
  45. Yang X, Li Y, Li Y, Ren X, Zhang X, Hu D, Gao Y, Shang H. Oxidative stress-mediated atherosclerosis: mechanisms and therapies. Front Physiol. 8: 600 (2017) https://doi.org/10.3389/fphys.2017.00600
  46. Yu Y, Feng XL, Gao H, Xie ZL, Dai Y, Huang XJ, Kurihara H, Ye WC, Zhong Y, Yao XS. Chemical constituents from the fruits of Gardenia jasminoides Ellis. Fitoterapia 83: 563-567 (2012) https://doi.org/10.1016/j.fitote.2011.12.027
  47. Zhang H, Lai Q, Li Y, Liu Y, Yang M. Learning and memory improvement and neuroprotection of Gardenia jasminoides (Fructus gardenia) extract on ischemic brain injury rats. J. Ethnopharmacol. 196: 225-235 (2017) https://doi.org/10.1016/j.jep.2016.11.042

Acknowledgement

Supported by : 세명대학교