Protective Effects of Lipophilic Extracts from Different Colored Paprikas on Inhibition of $H_2O_2$-induced Gap Junctional Intercellular Communications

$H_2O_2$로 유도된 WB-F344 세포의 GJIC 억제에 대한 색상별 파프리카 추출물의 보호 효과

  • Kim, Ji-Sun (Food and Nutrition in Home Economics, College of Natural Sciences, Korea National Open University) ;
  • Kim, Suna (Food and Nutrition in Home Economics, College of Natural Sciences, Korea National Open University)
  • 김지선 (한국방송통신대학교 자연과학대학 가정학과 식품영양전공) ;
  • 김선아 (한국방송통신대학교 자연과학대학 가정학과 식품영양전공)
  • Received : 2014.05.29
  • Accepted : 2014.06.12
  • Published : 2014.06.30

Abstract

This study analyzed phytochemicals, including various carotenoids, tocopherol and L-ascorbic acid, in green, yellow and orange paprikas (GP, YP and OP) and measured the preventive effects of lipophilic extracts from different colored paprikas on the blockage of gap junctional intercellular communication (GJIC), which is known as a cellular event associated with tumor promotion. Main carotenoids were lutein and ${\beta}$-carotene in GP, lutein, ${\beta}$-carotene, capsanthin, violaxanthin, ${\beta}$-carotene and capsorubin in YP, and lutein, ${\beta}$-carotene, cryptoxanthin and zeaxanthin in OP. Total carotenoid contents were $65.54{\pm}15.87$ mg/100 g dw in OP, $11.98{\pm}0.69$ mg/100 g dw in YP and $10.30{\pm}1.43$ mg/100 g dw in GP. Tocopherol contents were highest in GP compared with in YP and OP, whereas L-ascorbic acid contents were very high in all paprikas. We determined the non-cytotoxic levels of paprika extracts by MTT assay, which showed less formation of reactive oxygen species (ROS) induced by $500{\mu}M$ $H_2O_2$ for 1h. Finally, we showed that pretreatment of paprika extracts prevented inhibition of GJIC induced by $500{\mu}M$ $H_2O_2$ by the scrape-loading/dye-transfer technique. In conclusion, each colored paprika has unique phytochemicals and showed a protective effect on inhibition of GJIC.

Keywords

References

  1. Aizawa K, Inakuma T (2009) Dietary capsanthin, the main carotenoid in paprika(Capsicum annuum), alters plasma high-density lipoprotein-cholesterol levels and hepatic gene expression in rats. Brit J Nutr 102: 1760-1766. https://doi.org/10.1017/S0007114509991309
  2. Aizawa K, Matsumoto T, Inakuma T, Ishijima T, Nakai Y, Abe K, Amano F (2009) Administration of tomato and paprika beverages modifies hapatic glucose and lipid metabolism in mice: A DNA microarray analysis. J Agr Food Chem 57: 10964-10971. https://doi.org/10.1021/jf902401u
  3. Camera B, Moneger R (1978) Free and esterified carotenoids in green and red fruits of Capsicum annuum. Phytochem 17: 91-93. https://doi.org/10.1016/S0031-9422(00)89686-7
  4. Campbell SE, Stone WI, Whaley SG, Qui M, Krishnan K (2003) Gamma($\gamma$) tocopherol upregulates peroxisome proliferator activated receptor(PPAR) gamma($\gamma$) expression in SW 480 human colon cancer cell lines. BMC Cancer 3: 1-13. https://doi.org/10.1186/1471-2407-3-1
  5. Cerutti PA (1985) Prooxidant states and tumor promotion. Science 227: 375-381. https://doi.org/10.1126/science.2981433
  6. Cho JH, Cho SD, Hu H, Kim SH, Lee SK, Lee YS, Kang KS (2002) The roles of ERK1/2 and p38 MAP kinases in the preventive mechanisms of mushroom Phellinus linteus against the inhibition of gap junctional intercellular communication by hydrogen peroxide. Carcinogenesis 23: 1163-1169. https://doi.org/10.1093/carcin/23.7.1163
  7. Choi SJ, Kim SW, Lee JB, Lim HJ, Kim YJ, Tian C, So HS, Park R, Choung YH (2013) Gingko biloba extracts protect auditory hair cells from cisplatin-induced ototoxicity by inhibiting perturbation of gap junctional intercellular communication. Neuroscience 6: 49-61.
  8. Craft NE, Wise SA (1994) Individual carotenoid content of SRM 1548 total diet and influence of storage carotenoids. J Agric Food Chem 41: 208-213.
  9. Dwyer JH, Navab M, Dwyer KM, Hassan K, Sun P, Shircore A, Hama-Levy S, Hough G, Wang X, Drake T, Merz CN, Fogelman AM (2001) Oxygenated carotenoid lutein and progression of early atherosclerosis: The Los Angeles atherosclerosis study. Circulation 103: 2922-2927. https://doi.org/10.1161/01.CIR.103.24.2922
  10. El-Fouly MH, Trosko JE, Chang CC (1987) Scrape-loading and dye transfer: A rapid and simple technique to study gap junctional intercellulsr communication. Exp Cell Res 168: 422-430. https://doi.org/10.1016/0014-4827(87)90014-0
  11. Hwang JW, Park JS, Jo EH, Kim SJ, Yoon BS, Kim SH, Lee YS, Kang KS (2005) Chinese cabbage extracts and sulforaphane can protect $H_{2}O_{2}$-induced inhibition of gap junctional intercellular communication through the inactivation of ERK 1/2 and p38 MAP kinases. J Agric Food Chem 53: 8205-8210. https://doi.org/10.1021/jf051747h
  12. Jeong CH, Ko WH, Cho JR, Ahn CG, Shim KH (2006) Chemical components of Korean paprika according to cultivars. Korean J Food Preserv 13: 43-9.
  13. Jeong EM, Kim WT, Kim SR, Yun SH (2008) The actual condition and subjects of paprika in Korea. Munwonsa, Korea: Korea Rural Economic Insti. pp 2008-2022.
  14. Kang KS, Kang BC, Lee BJ, Che JH, Li GX, Trosko JE, Lee YS (2000) Preventive effect of epicatechin and ginsenoside Rb(2) on the inhibition of gap junctional intercellular communication by TPA and $H_{2}O_{2}$. Cancer Lett 152: 97-106. https://doi.org/10.1016/S0304-3835(99)00438-3
  15. Kang KS, Yun JW, Yoon B, Lim YK, Lee YS (2000). Preventive effect of germanium dioxide on the inhibition of gap junctional intercellular communication by TPA. Cancer Lett 152: 97-106. https://doi.org/10.1016/S0304-3835(99)00438-3
  16. KFDA (2003) Test method in general. J. Food Code Separate Volume.
  17. Kim JH, Lee BK, Lee KW, Lee HJ (2009) Resveratrol counteracts gallic acid-induced down-regulation of gap-junction intercellular communication. J Nutr Biochem 20: 149-154. https://doi.org/10.1016/j.jnutbio.2008.01.008
  18. Kim JS, Ahn J, Ha TY, Rhee HC, Kim S (2011) Comparison of phytochemical and antioxidant activities in different color stages and varieties of paprika harvested in Korea. Korean J Food Sci Technol 43: 564-569. https://doi.org/10.9721/KJFST.2011.43.5.564
  19. Kim JS, Ahn J, Lee SJ, Moon B, Ha TY, Kim S (2011) Phy tochemicals and antioxidant activity of fruits and leaves of paprika(Capsicum Annuum L., Var. Special) cultivated in Korea. J Food Sci 76: C193-198. https://doi.org/10.1111/j.1750-3841.2010.01891.x
  20. Kim JS, Ha TY, Ahn J, Kim HK, Kim S (2009) Pterostilbene from Vitis coignetiae protect $H_{2}O_{2}$-induced inhibition of gap junctional intercellular communication in rat liver cell line. Food Chem Toxicol 47: 202-209.
  21. Kontush A, Spranger T, Reich A, Baum K, Beisiegel U (1999) Lipophilic antioxidants in blood plasma as markers of atherosclerosis: the role of $\alpha$-carotene and $\gamma$-tocopherol. Atherosclerosis 144: 117-122.
  22. Kumar NM, Gilula NB (1996) The gap junction communication channel. Cell 84: 381-388. https://doi.org/10.1016/S0092-8674(00)81282-9
  23. Lee DE, Shin BJ, Hur HJ, Kim JH, Kim J, Kang NJ, Kim DO, Lee CY, Lee KW, Lee HJ (2010) Quercetin, the active phenolic component in kiwifruit, prevents hydrogen peroxideinduced inhibition of gap-junction intercellular communication. Br J Nutr 104: 164-170. https://doi.org/10.1017/S0007114510000346
  24. Loewenstein WR (1981) Junctional intercellular communication: the cell-to-cell membrane channel. Physiol Rev 61: 829-913.
  25. Maoka T, Enjo F, Tokuda H, Nishino H (2004) Biological function and cancer prevention by paprika carotenoids. Foods Food Ingred J Jpn 209: 203-210.
  26. Matsufuji H, Ishikawa K, Nunomura O, Chino M, Takeda M (2007) Anti-oxidant content of different coloured sweet peppers, white, green, yellow, orange and red (Capsicum annuum L.) Int J Food Sci Tech 42: 1482-1488. https://doi.org/10.1111/j.1365-2621.2006.01368.x
  27. Matsufuji H, Nakamura H, Chino M, Takeda M (1998) Antioxidant activity of capsanthin and the fatty acid esters in paprika (Capsicum annuum). J Agric Food Chem 46: 3468-3472. https://doi.org/10.1021/jf980200i
  28. Matus Z, Deli J, Szabolcs J (1991) Carotenoid composition of yellow pepper during ripening: isolation of $\beta$-cryptoxanthin 5,6-epoxide. J Agric Food Chem 39: 1907-1914. https://doi.org/10.1021/jf00011a003
  29. Minguez-Mosquera, MI, Hornero-Mendez D (1994) Changes in carotenoid esterification during the fruit ripening of Capsicum annuum cv. Bola. J Agric Food Chem 42: 640-644. https://doi.org/10.1021/jf00039a007
  30. Saez JC, Connor JA, Spray DC, Bennett MV (1989) Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate and to calcium ions. P Natl Acad Sci. USA 86: 2708-2712. https://doi.org/10.1073/pnas.86.8.2708
  31. Sedden JM, Ajani UA, Sperduto RD, Hiller R, Blair N, Burton TC, Farber MD, Gragoudas ES, Haller J, Miller DT, Yannuzi LA, Willet W (1994) Dietary carotenoids, vitamin A, C and E, and advanced age-related macular degeneration. J Am Med Assoc 272: 1413-1420. https://doi.org/10.1001/jama.1994.03520180037032
  32. Surh YJ (2003) Cancer chemoprevention with dietary phytochemicals. Nautre 3: 768-780.
  33. Upham BL, Kang KS, Cho HY, Trosko JE (1997) Hydrogen peroxide inhibits gap junctional intercellular communication in glutathione sufficient but not glutathione deficient cells. Carcinogenesis 18: 37-42.
  34. Weller P, Breithaupt, DE (2003) Identification and quantification of zeaxanthin esters in plants using liquid chromatographymass spectrometry. J Agric Food Chem 51: 7044-7049. https://doi.org/10.1021/jf034803s