Advanced SearchSearch Tips
Inhibitory Effects of Spinach, Cabbage, and Onion Extracts on Growth of Cancer Cells
facebook(new window)  Pirnt(new window) E-mail(new window) Excel Download
 Title & Authors
Inhibitory Effects of Spinach, Cabbage, and Onion Extracts on Growth of Cancer Cells
Lee, Hae-Nim; Shin, Seong-Ah; Choo, Gang-Sik; Kim, Hyeong-Jin; Park, Young-Seok; Kim, Sang-Ki; Jung, Ji-Youn;
  PDF(new window)
Extracts from spinach, cabbage, and onion are known to possess various instructive characteristics, including antioxidant and anti-inflammation activities. Spinach, cabbage, and onion are consumed worldwide and represent important sources of dietary phytochemicals with proven antioxidant properties, such as flavonoids and phenolic acids. Food-derived flavonoids and phenolic compounds are expected to be promising drugs for cancer. In the present study, we investigated the effects of methanol extracts of spinach, cabbage, and onion on cell proliferation and apoptosis in human gastric and breast cancer cells. Proliferation rates of AGS, MDA-MB-231, and SK-BR-3 cells were determined by 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay. The methanol extracts of spinach, cabbage, and onion inhibited proliferation of cancer cells in a dose-dependent manner. 4',6-Diamidino-2-phenylindole (DAPI) staining revealed that chromatin condensation significantly increased compared with the control. In the results of MTT assay and DAPI staining, onion extract was the most effective in inhibiting cancer cell proliferation and apoptosis. To assess changes in protein expression level by onion extract, we identified Bax (pro-apoptotic), Bcl-2 (anti-apoptotic), and poly(ADP-ribose) polymerase (PARP) protein by western blot analysis. The expression of Bax and cleaved-PARP increased, whereas expression of Bcl-2 was decreased compared with the control. These results suggest that spinach, cabbage, and onion extracts suppressed growth of human gastric cancer AGS, human breast cancer MDA-MB-231, and SK-BR-3 cells through induction of apoptosis. Among the extracts, onion extract had stronger anti-cancer and apoptosis induction effects than spinach and cabbage extracts. Further, onion extract more effectively induced apoptosis of human gastric cancer cells than human breast cancer cells. Therefore, further studies are needed to determine the anti-cancer effects of onion extracts in vivo. Onion extract can be developed as a chemopreventive or therapeutic agent for gastric cancer.
 Cited by
Kang HI, Kim JY, Cho HD, Park KW, Kang JS, Seo KI. 2010. Resveratrol induces apoptosis in primary human prostate cancer cells. J Korean Soc Food Sci Nutr 39: 1119-1125. crossref(new window)

Lee MS, Cha EY, Thuong PT, Kim JY, Ahn MS, Sul JY. 2010. Down-regulation of human epidermal growth factor receptor 2/neu oncogene by corosolic acid induces cell cycle arrest and apoptosis in NCI-N87 human gastric cancer cells. Biol Pharm Bull 33: 931-937. crossref(new window)

Li N, Fan LL, Sun GP, Wan XA, Wang ZG, Wu Q, Wang H. 2010. Paeonol inhibits tumor growth in gastric cancer in vitro and in vivo. World J Gastroenterol 16: 4483-4490. crossref(new window)

Zhang L, Hou YH, Wu K, Zhai JS, Lin N. 2010. Proteomic analysis reveals molecular biological details in varioliform gastritis without Helicobacter pylori infection. World J Gastroenterol 16: 3364-3673.

NCC. Annual report of cancer statistics in Korea in 2012. (accessed Dec 2014).

Dorssers LCJ, van der Flier S, Brinkman A, van Agthoven T, Veldscholte J, Berns EMJJ, Klijn JGM, Beex L, Foekens JA. 2001. Tamoxifen resistance in breast cancer. Drugs 61: 1721-1733. crossref(new window)

Seeram NP. 2008. Berry fruits for cancer prevention: current status and future prospects. J Agric Food Chem 56: 630-635. crossref(new window)

Dorai T, Aggarwal BB. 2004. Role of chemopreventive agents in cancer therapy. Cancer Lett 215: 129-140. crossref(new window)

Nkondjock A, Ghadirian P. 2005. Risk factors and risk reduction of breast cancer. Med Sci (Paris) 21: 175-180. crossref(new window)

Ogimoto I, Shibata A, Fukuda K. 2000. World Cancer Research Fund/American Institute of Cancer Research 1997 Recommendations: applicability to digestive tract cancer in Japan. Cancer Causes Control 11: 9-23. crossref(new window)

Block G, Patterson B, Subar A. 1992. Fruits, vegetables and cancer prevention: a review of the epidemiological evidence. Nutr Cancer 18: 1-29. crossref(new window)

Bravo L. 1998. Polyphenols: chemistry, dietary sources, metabolism, and nutritional significance. Nutr Rev 56: 317-333.

Naderi GA, Asgary S, Sarraf-Zadegan N, Shirvany H. 2003. Anti-oxidant effect of flavonoids on the susceptibility of LDL oxidation. Mol Cell Biochem 246: 193-196. crossref(new window)

Cragg GM, Newman DJ. 2005. Plants as a source of anticancer agents. J Ethnopharmacol 100: 72-79. crossref(new window)

Kaul TN, Middleton E Jr, Ogra PL. 1985. Antiviral effect of flavonoids on human viruses. J Med Virol 15: 71-79. crossref(new window)

Hamalainen M, Nieminen R, Vuorela P, Heinonen M, Moilanen E. 2007. Anti-inflammatory effects of flavonoids: genistein, kaempferol, quercetin, and daidzein inhibit STAT-1 and NF-${\kappa}B$ activations, whereas flavone, isorhamnetin, naringenin, and pelargonidin inhibit only NF-${\kappa}B$ activation along with their inhibitory effect on iNOS expression and NO production in activated macrophages. Mediators Inflammation 2007: 45673.

Manach C, Scalbert A, Morand C, Remesy C, Jimenez L. 2004. Polyphenols: food sources and bioavailability. Am J Clin Nutr 79: 727-747. crossref(new window)

Ko EY, Nile SH, Sharma K, Li GH, Park SW. 2015. Effect of different exposed lights on quercetin and quercetin glucoside content in onion (Allium cepa L.). Saudi J Biol Sci 22: 398-403. crossref(new window)

Sultana B, Anwar F. 2008. Flavonols (kaempeferol, quercetin, myricetin) contents of selected fruits, vegetables and medicinal plants. Food Chem 108: 879-884. crossref(new window)

Nile SH, Park SW. 2013. Total phenolics, antioxidant and xanthine oxidase inhibitory activity of three colored onions (Allium cepa L.). Front Life Sci 7: 224-228. crossref(new window)

Lee MH, Han JS, Kozukue N, Minamide T. 2005. Physicochemical characteristics of commercial spinach produced in autumn. J East Asian Soc Dietary Life 15: 306-314.

Kim NY, Yoon SK, Jang MS. 1993. Effect of blanching on the chemical properties of different kind of spinach. Korean J Soc Food Sci 9: 204-209.

Lee YA, Kim HY, Cho EJ. 2005. Comparison of methanol extracts from vegetables on antioxidative effect under in vitro and cell system. J Korean Soc Food Sci Nutr 34: 1151-1156. crossref(new window)

Matsubara K, Matsumoto H, Mizushina Y, Mori M, Nakajima N, Fuchigami M, Yoshida H, Hada T. 2005. Inhibitory effect of glycolipids from spinach on in vitro and ex vivo angiogenesis. Oncol Rep 14: 157-160.

Maeda N, Kokai Y, Ohtani S, Sahara H, Kumamoto-Yonezawa Y, Kuriyama I, Hada T, Sato N, Yoshida H, Mizushina Y. 2008. Anti-tumor effect of orally administered spinach glycolipid fraction on implanted cancer cells, colon-26, in mice. Lipids 43: 741-748. crossref(new window)

Jahangir M, Kim HK, Choi YH, Verpoorte R. 2009. Healthaffecting compounds in Brassicaceae. Comp Rev Food Sci Food Saf 8: 31-43. crossref(new window)

Sang JP, Minchinton IR, Johnstone PK, Truscott RJW. 1984. Glucosinolate profiles in the seed, root and leaf tissue of cabbage, mustard, rapeseed, radish and swede. Can J Plant Sci 64: 77-93. crossref(new window)

Singh J, Upadhyay AK, Bahadur A, Singh B, Singh KP, Rai M. 2006. Antioxidant phytochemicals in cabbage (Brassica oleracea L. var. capitata). Sci Hortic 108: 233-237. crossref(new window)

Mattila P, Hellstrom J. 2007. Phenolic acids in potatoes, vegetables, and some of their products. J Food Compos Anal 20: 152-160. crossref(new window)

Hwang ES, Hong E, Kim GH. 2012. Determination of bioactive compounds and anti-cancer effect from extracts of Korean cabbage and cabbage. Korean J Food & Nutr 25: 259-265. crossref(new window)

Hwang ES, Lee HJ. 2010. Effects of phenylethyl isothiocyanate and its metabolite on cell-cycle arrest and apoptosis in LNCaP human prostate cancer cells. Int J Food Sci Nutr 61: 324-336. crossref(new window)

Smith TK, Mithen R, Johnson IT. 2003. Effects of Brassica vegetable juice on the induction of apoptosis and aberrant crypt foci in rat colonic mucosal crypts in vivo. Carcinogenesis 24: 491-495. crossref(new window)

Cho J, Bae RN, Lee SK. 2010. Current research status of postharvest technology of onion (Allium cepa L.). Kor J Hort Sci Technol 28: 522-527.

Bilyk A, Cooper PL, Sapers GM. 1984. Varietal differences in distribution of quercetin and kaempferol in onion (Allium cepa L.) tissue. J Agric Food Chem 32: 274-276. crossref(new window)

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. crossref(new window)

Patil BS, Pike LM. 1995. Distribution of quercetin content in different rings of various coloured onion (Allium cepa L.) cultivars. J Hortic Sci 70: 643-650. crossref(new window)

Alpsoy S, Kanter M, Aktas C, Erboga M, Akyuz A, Akkoyun DC, Oran M. 2014. Protective effects of onion extract on cadmium-induced oxidative stress, histological damage, and apoptosis in rat heart. Biol Trace Elem Res 159: 297-303. crossref(new window)

Ola-Mudathir KF, Maduagwu EN. 2014. Antioxidant effects of methanol extract of Allium cepa linn on cyanide-induced renal toxicity in male Wistar rats. Niger J Physiol Sci 29: 147-151.

Kim J, Kim JS, Park E. 2013. Cytotoxic and anti-inflammatory effects of onion peel extract on lipopolysaccharide stimulated human colon carcinoma cells. Food Chem Toxicol 62: 199-204. crossref(new window)

Elnima EI, Ahmed SA, Mekkawi AG, Mossa JS. 1983. The antimicrobial activity of garlic and onion extracts. Pharmazie 38: 747-748.

Rho SN, Han JH. 2000. Cytotoxicity of garlic and onion methanol extract on human lung cancer cell lines. J Korean Soc Food Sci Nutr 29: 870-874.

Yang EJ, Kim GS, Kim JA, Song KS. 2013. Protective effects of onion-derived quercetin on glutamate-mediated hippocampal neuronal cell death. Pharmacogn Mag 9: 302-308. crossref(new window)

Lee HJ, Lee KH, Park E, Chung HK. 2010. Effect of onion extracts on serum cholesterol in borderline hypercholesterolemic participants. J Korean Soc Food Sci Nutr 39: 1783-1789. crossref(new window)

Wang Y, Tian WX, Ma XF. 2012. Inhibitory effects of onion (Allium cepa L.) extract on proliferation of cancer cells and adipocytes via inhibiting fatty acid synthase. Asian Pac J Cancer Prev 13: 5573-5579. crossref(new window)

Hong YJ, Kim SY, Han J, Lim YI, Park KY. 2013. Inhibitory effects of cabbage juice and cabbage-mixed juice on the growth of AGS human gastric cancer cells and on HCl-ethanol induced gastritis in rats. J Korean Soc Food Sci Nutr 42: 682-689. crossref(new window)

Hengartner MO. 2000. The biochemistry of apoptosis. Nature 407: 770-776. crossref(new window)

Wyllie AH, Kerr JF, Currie AR. 1980. Cell death: the significance of apoptosis. Int Rev Cytol 68: 251-306. crossref(new window)

Kim EJ, Park SY, Hong J, Shin M, Lim SS, Shin HK, Yoon JH. 2007. Inhibitory effect of the methanolic extract of Symphyocladia latiuscula on the growth of HT-29 human colon cancer cells. J Korean Soc Food Sci Nutr 36: 431-438. crossref(new window)

Donovan M, Cotter TG. 2004. Control of mitochondrial integrity by Bcl-2 family members and caspase-independent cell death. Biochim Biophys Acta 1644: 133-147. crossref(new window)

Oltvai ZN, Milliman CL, Korsmeyer SJ. 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programed cell death. Cell 74: 609-619. crossref(new window)

Galluzzi L, Kepp O, Trojel-Hansen C, Kroemer G. 2012. Mitochondrial control of cellular life, stress, and death. Circ Res 111: 1198-1207. crossref(new window)

Boulares AH, Yakovlev AG, Ivanova V, Stoica BA, Wang G, Iyer S, Smulson M. 1999. Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J Biol Chem 274: 22932-22940. crossref(new window)

Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, Poirier GG, Salvesen GS, Dixit VM. 1995. Yama/$CPP32{\beta}$, a mammalian homolog of CED-3, is a CrmAinhibitable protease that cleaves the death substrate poly (ADP-ribose) polymerase. Cell 81: 801-809. crossref(new window)

Los M, Mozoluk M, Ferrari D, Stepczynska A, Stroh C, Renz A, Herceg Z, Wang ZQ, Schulze-Osthoff K. 2002. Activation and caspase-mediated inhibition of PARP: a molecular switch between fibroblast necrosis and apoptosis in death receptor signaling. Mol Biol Cell 13: 978-988. crossref(new window)

Wiechmann L, Sampson M, Stempel M, Jacks LM, Patil SM, King T, Morrow M. 2009. Presenting features of breast cancer differ by molecular subtype. Ann Surg Oncol 16: 2705-2710. crossref(new window)

Shin JH, Kim HW, Lee MK, Lee SH, Lee YM, Jang HH, Hwang KA, Cho YS, Kim JB. 2014. Content and distribution of flavanols, flavonols and flavanones on the common vegetables in Korea. Korean J Environ Agric 33: 205-212. crossref(new window)