Preventive Nutrition and Food Science

The Korean Society of Food Science and Nutrition (한국식품영양과학회)
권호 표지
DOI QR코드

DOI QR Code

Protective Effects of Sweet Orange, Unshiu Mikan, and Mini Tomato Juice Powders on t-BHP-Induced Oxidative Stress in HepG2 Cells

  • Jannat, Susoma (Department of Food and Life Science, Pukyong National University) ;
  • Ali, Md Yousof (Department of Food and Life Science, Pukyong National University) ;
  • Kim, Hyeung-Rak (Department of Food and Life Science, Pukyong National University) ;
  • Jung, Hyun Ah (Department of Food Science and Human Nutrition, Chonbuk National University) ;
  • Choi, Jae Sue (Department of Food and Life Science, Pukyong National University)
  • Received : 2016.06.08
  • Accepted : 2016.07.10
  • Published : 2016.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

The aim of this study was to investigate the protective effects of juice powders from sweet orange [Citrus sinensis (L.) Osbeck], unshiu mikan (Citrus unshiu Marcow), and mini tomato (Solanum lycopersicum L.), and their major flavonoids, hesperidin, narirutin, and rutin in tert-butyl hydroperoxide (t-BHP)-induced oxidative stress in HepG2 cells. The increased reactive oxygen species and decreased glutathione levels observed in t-BHP-treated HepG2 cells were ameliorated by pretreatment with juice powders, indicating that the hepatoprotective effects of juice powders and their major flavonoids are mediated by induction of cellular defense against oxidative stress. Moreover, pretreatment with juice powders up-regulated phase-II genes such as heme oxygenase-1 (HO-1), thereby preventing cellular damage and the resultant increase in HO-1 expression. The high-performance liquid chromatography profiles of the juice powders confirmed that hesperidin, narirutin, and rutin were the key flavonoids present. Our results suggest that these fruit juice powders and their major flavonoids provide a significant cytoprotective effect against oxidative stress, which is most likely due to the flavonoid-related bioactive compounds present, leading to the normal redox status of cells. Therefore, these fruit juice powders could be advantageous as bioactive sources for the prevention of oxidative injury in hepatoma cells.

Keywords

References

  1. Breimer LH. 1990. Molecular mechanisms of oxygen radical carcinogenesis and mutagenesis: the role of DNA base damage. Mol Carcinog 3: 188-197.
  2. Rushmore TH, Kong ANT. 2002. Pharmacogenomics, regulation and signaling pathways of phase I and II drug metabolizing enzymes. Curr Drug Metab 3: 481-490. https://doi.org/10.2174/1389200023337171
  3. Kapitulnik J. 2004. Bilirubin: an endogenous product of heme degradation with both cytotoxic and cytoprotective properties. Mol Pharmacol 66: 773-779. https://doi.org/10.1124/mol.104.002832
  4. Alam J, Cook JL. 2003. Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des 9: 2499-2511. https://doi.org/10.2174/1381612033453730
  5. Morse D, Choi AMK. 2002. Heme oxygenase-1: the "emerging molecule" has arrived. Am J Respir Cell Mol Biol 27: 8-16. https://doi.org/10.1165/ajrcmb.27.1.4862
  6. Sies H. 1999. Glutathione and its role in cellular functions. Free Radic Biol Med 27: 916-921. https://doi.org/10.1016/S0891-5849(99)00177-X
  7. Wang H, Liu H, Liu RM. 2003. Gender difference in glutathione metabolism during aging in mice. Exp Gerontol 38: 507-517. https://doi.org/10.1016/S0531-5565(03)00036-6
  8. Yoshida K, Hirokawa J, Tagami S, Kawakami Y, Urata Y, Kondo T. 1995. Weakened cellular scavenging activity against oxidative stress in diabetes mellitus: regulation of glutathione synthesis and efflux. Diabetologia 38: 201-210. https://doi.org/10.1007/BF00400095
  9. Tripoli E, La Guardia M, Giammanco S, Di Majo D, Giammanco M. 2007. Citrus flavonoids: molecular structure, biological activity and nutritional properties: a review. Food Chem 104: 466-479. https://doi.org/10.1016/j.foodchem.2006.11.054
  10. Niu LY, Wu JH, Liao XJ, Chen F, Wang ZF, Zhao GH, Hu XS. 2008. Physicochemical characteristics of orange juice samples from seven cultivars. Agric Sci China 7: 41-47. https://doi.org/10.1016/S1671-2927(08)60020-6
  11. Cesar TB, Aptekmann NP, Araujo MP, Vinagre CC, Maranhao RC. 2010. Orange juice decreases low-density lipoprotein cholesterol in hypercholesterolemic subjects and improves lipid transfer to high-density lipoprotein in normal and hypercholesterolemic subjects. Nutr Res 30: 689-694. https://doi.org/10.1016/j.nutres.2010.09.006
  12. Etebu E, Nwauzoma AB. 2014. A review on sweet orange (Citrus sinensis L Osbeck): health, diseases and management. Am J Res Commun 2: 33-70.
  13. Kang SI, Shin HS, Kim HM, Hong YS, Yoon SA, Kang SW, Kim JH, Kim MH, Ko HC, Kim SJ. 2012. Immature Citrus sunki peel extract exhibits antiobesity effects by ${\beta}$-oxidation and lipolysis in high-fat diet-induced obese mice. Biol Pharm Bull 35: 223-230. https://doi.org/10.1248/bpb.35.223
  14. Park HJ, Jung UJ, Cho SJ, Jung HK, Shim S, Choi MS. 2013. Citrus unshiu peel extract ameliorates hyperglycemia and hepatic steatosis by altering inflammation and hepatic glucose- and lipid-regulating enzymes in db/db mice. J Nutr Biochem 24: 419-427. https://doi.org/10.1016/j.jnutbio.2011.12.009
  15. Sun Y, Wang J, Gu S, Liu Z, Zhang Y, Zhang X. 2010. Simultaneous determination of flavonoids in different parts of Citrus reticulata 'Chachi' fruit by high performance liquid chromatography-photodiode array detection. Molecules 15: 5378-5388. https://doi.org/10.3390/molecules15085378
  16. Kootstra A. 1994. Protection from UV-B-induced DNA damage by flavonoids. Plant Mol Biol 26: 771-774. https://doi.org/10.1007/BF00013762
  17. Lin N, Sato T, Takayama Y, Mimaki Y, Sashida Y, Yano M, Ito A. 2003. Novel anti-inflammatory actions of nobiletin, a citrus polymethoxy flavonoid, on human synovial fibroblasts and mouse macrophages. Biochem Pharmacol 65: 2065-2071. https://doi.org/10.1016/S0006-2952(03)00203-X
  18. Kobayashi S, Tanabe S. 2006. Evaluation of the anti-allergic activity of Citrus unshiu using rat basophilic leukemia RBL-2H3 cells as well as basophils of patients with seasonal allergic rhinitis to pollen. Int J Mol Med 17: 511-515.
  19. Di Majo D, Giammanco M, La Guardia M, Tripoli E, Giammanco S, Finotti E. 2005. Flavanones in Citrus fruit: structure-antioxidant activity relationships. Food Res Int 38: 1161-1166. https://doi.org/10.1016/j.foodres.2005.05.001
  20. Bracke M, Vyncke B, Opdenakker G, Foidart JM, De Pestel G, Mareel M. 1991. Effect of catechins and citrus flavonoids on invasion in vitro. Clin Exp Metastasis 9: 13-25. https://doi.org/10.1007/BF01831706
  21. Manach C, Regerat F, Texier O, Agullo G, Demigne C, Remesy C. 1996. Bioavailability, metabolism and physiological impact of 4-oxo-flavonoids. Nutr Res 16: 517-544. https://doi.org/10.1016/0271-5317(96)00032-2
  22. Rosales MA, Cervilla LM, Sanchez-Rodriguez E, Rubio-Wilhelmi Mdel M, Blasco B, Rios JJ, Soriano T, Castilla N, Romero L, Ruiz JM. 2011. The effect of environmental conditions on nutritional quality of cherry tomato fruits: evaluation of two experimental Mediterranean greenhouses. J Sci Food Agric 91: 152-162. https://doi.org/10.1002/jsfa.4166
  23. Raiola A, Rigano MM, Calafiore R, Frusciante L, Barone A. 2014. Enhancing the health-promoting effects of tomato fruit for biofortified food. Mediators Inflammation 2014: 139873.
  24. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63. https://doi.org/10.1016/0022-1759(83)90303-4
  25. Lebel CP, Bondy SC. 1990. Sensitive and rapid quantitation of oxygen reactive species formation in rat synaptosomes. Neurochem Int 17: 435-440. https://doi.org/10.1016/0197-0186(90)90025-O
  26. Choi JS, Han YR, Byeon JS, Choung SY, Sohn HS, Jung HA. 2015. Protective effect of fucosterol isolated from the edible brown algae, Ecklonia stolonifera and Eisenia bicyclis, on tert-butyl hydroperoxide- and tacrine-induced HepG2 cell injury. J Pharm Pharmacol 67: 1170-1178. https://doi.org/10.1111/jphp.12404
  27. Doll R. 1990. An overview of the epidemiological evidence linking diet and cancer. Proc Nutr Soc 49: 119-131. https://doi.org/10.1079/PNS19900018
  28. Willett WC. 1994. Diet and health: what should we eat?. Science 264: 532-537. https://doi.org/10.1126/science.8160011
  29. Kris-Etherton PM, Hecker KD, Bonanome A, Coval SM, Binkoski AE, Hilpert KF, Griel AE, Etherton TD. 2002. Bioactive compounds in foods: their role in the prevention of cardiovascular disease and cancer. Am J Med 113: 71-88. https://doi.org/10.1016/S0002-9343(01)00995-0
  30. Aschoff JK, Kaufmann S, Kalkan O, Neidhart S, Carle R, Schweiggert RM. 2015. In vitro bioaccessibility of carotenoids, flavonoids, and vitamin C from differently processed oranges and orange juices [Citrus sinensis (L.) Osbeck]. J Agric Food Chem 63: 578-587. https://doi.org/10.1021/jf505297t
  31. Aptekmann NP, Cesar TB. 2013. Long-term orange juice consumption is associated with low LDL-cholesterol and apolipoprotein B in normal and moderately hypercholesterolemic subjects. Lipids Health Dis 12: 119. https://doi.org/10.1186/1476-511X-12-119
  32. Foroudi S, Potter AS, Stamatikos A, Patil BS, Deyhim F. 2014. Drinking orange juice increases total antioxidant status and decreases lipid peroxidation in adults. J Med Food 17: 612-617. https://doi.org/10.1089/jmf.2013.0034
  33. Ghanim H, Sia CL, Upadhyay M, Korzeniewski K, Viswanathan P, Abuaysheh S, Mohanty P, Dandona P. 2010. Orange juice neutralizes the proinflammatory effect of a high-fat, high-carbohydrate meal and prevents endotoxin increase and Toll-like receptor expression. Am J Clin Nutr 91: 940-949. https://doi.org/10.3945/ajcn.2009.28584
  34. Giovannucci E. 1999. Tomatoes, tomato-based products, lycopene, and cancer: review of the epidemiologic literature. J Natl Cancer Inst 91: 317-331. https://doi.org/10.1093/jnci/91.4.317
  35. Crozier A, Lean MEJ, McDonald MS, Black C. 1997. Quantitative analysis of the flavonoid content of commercial tomatoes, onions, lettuce, and celery. J Agric Food Chem 45: 590-595. https://doi.org/10.1021/jf960339y
  36. Stewart AJ, Bozonnet S, Mullen W, Jenkins GI, Lean MEJ, Crozier A. 2000. Occurrence of flavonols in tomatoes and tomato-based products. J Agric Food Chem 48: 2663-2669. https://doi.org/10.1021/jf000070p
  37. Raiola A, Giudice RD, Monti DM, Tenore GC, Barone A, Rigano MM. 2016. Bioactive compound content and cytotoxic effect on human cancer cells of fresh and processed yellow tomatoes. Molecules 21: 33.
  38. Cenariu D, Pintea A, Fischer-Fodor E, Bucak MN, Cenariu M, Crisan G. 2015. Cytotoxic potential of antioxidants from tomatoes on tumoral cells. Bull Univ Agric Sci Vet Med Cluj-Napoca Vet Med 72: 401-405.
  39. Chen RY, Wu JJ, Tsai MJ, Liu MS. 2000. Effect of storage and thermal treatment on the antioxidant activity of tomato fruits. J Chin Agric Chem Soc 38: 353-360.
  40. Wang H, Cao G, Prior RL. 1996. Total antioxidant capacity of fruits. J Agric Food Chem 44: 701-705. https://doi.org/10.1021/jf950579y
  41. Chang CH, Lin HY, Chang CY, Liu YC. 2006. Comparisons on the antioxidant properties of fresh, freeze-dried and hot-air-dried tomatoes. J Food Eng 77: 478-485. https://doi.org/10.1016/j.jfoodeng.2005.06.061
  42. Yen GC, Yeh CT, Chen YJ. 2004. Protective Effect of Mesona procumbens against tert-butyl hydroperoxide-induced acute hepatic damage in rats. J Agric Food Chem 52: 4121-4127. https://doi.org/10.1021/jf049840d
  43. Garcia-Alonso J, Ros G, Periago MJ. 2006. Antiproliferative and cytoprotective activities of a phenolic-rich juice in HepG2 cells. Food Res Int 39: 982-991. https://doi.org/10.1016/j.foodres.2006.07.001
  44. Williams GM, Jeffrey AM. 2000. Oxidative DNA damage: endogenous and chemically induced. Regul Toxicol Pharmacol 32: 283-292. https://doi.org/10.1006/rtph.2000.1433
  45. Minotti G, Borrello S, Palombini G, Galeotti T. 1986. Cytochrome P-450 deficiency and resistance to t-butyl hydroperoxide of hepatoma microsomal lipid peroxidation. Biochim Biophys Acta 876: 220-225. https://doi.org/10.1016/0005-2760(86)90277-8
  46. Luper S. 1998. A review of plants used in the treatment of liver disease: part 1. Altern Med Rev 3: 410-421.
  47. Alia M, Romos S, Mateos R, Bravo L, Goya L. 2005. Response of the antioxidant defense system to tert-butyl hydroperoxide and hydrogen peroxide in a human hepatoma cell line (HepG2). J Biochem Mol Toxicol 19: 119-128. https://doi.org/10.1002/jbt.20061
  48. Kaliora AC, Dedoussis GV, Schmidt H. 2006. Dietary antioxidants in preventing atherogenesis. Atherosclerosis 187: 1-17. https://doi.org/10.1016/j.atherosclerosis.2005.11.001
  49. Chen ZT, Chu HL, Chyau CC, Chu CC, Duh PD. 2012. Protective effects of sweet orange (Citrus sinensis) peel and their bioactive compounds on oxidative stress. Food Chem 135: 2119-2127. https://doi.org/10.1016/j.foodchem.2012.07.041
  50. Anderson ME. 1985. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113: 548-555. https://doi.org/10.1016/S0076-6879(85)13073-9
  51. Yu HM, Wang BS, Chu HL, Chang LW, Yen WJ, Lin CJ, Duh PD. 2007. Napiergrass (Pennisetum purpureum S.) protects oxidative damage of biomolecules and modulates antioxidant enzyme activity. Food Chem 105: 1364-1374. https://doi.org/10.1016/j.foodchem.2007.05.003
  52. Choi AM, Alam J. 1996. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 15: 9-19. https://doi.org/10.1165/ajrcmb.15.1.8679227
  53. Ryter SW, Otterbein LE, Morse D, Choi AM. 2002. Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol Cell Biochem 234-235: 249-263. https://doi.org/10.1023/A:1015957026924
  54. Qaisiya M, Coda Zabetta CD, Bellarosa C, Tiribelli C. 2014. Bilirubin mediated oxidative stress involves antioxidant response activation via Nrf2 pathway. Cell Signal 26: 512-520. https://doi.org/10.1016/j.cellsig.2013.11.029
  55. Rizzo V, Clifford MN, Brown JE, Siracusa L, Muratore G. 2016. Effects of processing on the polyphenol and phenolic acid content and antioxidant capacity of semi-dried cherry tomatoes (Lycopersicon esculentum M.). J Sci Food Agric 96: 2040-2046. https://doi.org/10.1002/jsfa.7315
  56. Garg A, Garg S, Zaneveld LJ, Singla AK. 2001. Chemistry and pharmacology of the citrus bioflavonoid hesperidin. Phytother Res 15: 655-669. https://doi.org/10.1002/ptr.1074
  57. Emim JA, Oliveira AB, Lapa AJ. 1994. Pharmacological evaluation of the anti-inflammatory activity of a citrus bioflavonoid, hesperidin, and the isoflavonoids, duartin and claussequinone, in rats and mice. J Pharm Pharmacol 46: 118-122. https://doi.org/10.1111/j.2042-7158.1994.tb03753.x
  58. Lim H, Yeo E, Song E, Chang YH, Han BK, Choi HJ, Hwang J. 2015. Bioconversion of Citrus unshiu peel extracts with cytolase suppresses adipogenic activity in 3T3-L1 cells. Nutr Res Pract 9: 599-605. https://doi.org/10.4162/nrp.2015.9.6.599
  59. Funaguchi N, Ohno Y, La BL, Asai T, Yuhgetsu H, Sawada M, Takemura G, Minatoguchi S, Fujiwara T, Fujiwara H. 2007. Narirutin inhibits airway inflammation in an allergic mouse model. Clin Exp Pharmacol Physiol 34: 766-770. https://doi.org/10.1111/j.1440-1681.2007.04636.x
  60. Park HY, Ha SK, Eom H, Choi I. 2013. Narirutin fraction from citrus peels attenuates alcoholic liver disease in mice. Food Chem Toxicol 55: 637-644. https://doi.org/10.1016/j.fct.2013.01.060
  61. Arima H, Ashida H, Danno G. 2002. Rutin-enhanced antibacterial activities of flavonoids against Bacillus cereus and Salmonella enteritidis. Biosci Biotechnol Biochem 66: 1009-1014. https://doi.org/10.1271/bbb.66.1009
  62. Kessler M, Ubeaud G, Jung L. 2003. Anti- and pro-oxidant activity of rutin and quercetin derivatives. J Pharm Pharmacol 55: 131-142. https://doi.org/10.1211/002235702559
  63. Baldisserotto A, Vertuani S, Bino A, De Lucia D, Lampronti I, Milani R, Gambari R, Manfredini S. 2015. Design, synthesis and biological activity of a novel Rutin analogue with improved lipid soluble properties. Bioorg Med Chem 23: 264-271. https://doi.org/10.1016/j.bmc.2014.10.023

Cited by

  1. Hepatoprotective effects of different combinations of sweet orange, Unshiu mikan, and mini tomato juice powders against tert- butyl hydroperoxide-induced oxidative stress in HepG2 cells vol.41, pp.3, 2017, https://doi.org/10.1111/jfbc.12369
  2. Effect of chemical preservatives on the shelf life of tomato juice vol.3, pp.2, 2019, https://doi.org/10.2478/acmy-2019-0006
  3. Dietary immature Citrus unshiu alleviates UVB- induced photoaging by suppressing degradation of basement membrane in hairless mice vol.6, pp.6, 2016, https://doi.org/10.1016/j.heliyon.2020.e04218