Variations in Free Radical Scavenging Capacity and Antiproliferative Activity Among Different Genotypes of Autumn Olive (Elaeagnus umbellata)

Abstract

Fruit from six genotypes of autumn olive (Elaeagnus umbellata Thunb.) (‘Brilliant Rose’, ‘Delightful’, ‘Jewel’, Natural 1, Natural 2, and ‘Sweet Tart’) were evaluated for antioxidant capacity and anti-cancer properties. Based on data from electron spin resonance (ESR) measurements, autumn olive contained potent free radical scavenging activities for hydroxyl (·OH) and superoxide (O₂·-) radicals. Among the six genotypes, ‘Brilliant Rose’ and ‘Jewel’ had the highest levels of antioxidant activity. Pretreatment of JG6 P⁺ mouse epidermal cells with autumn olive extracts inhibited the activation of activator protein-1 (AP-1) and nuclear factor-kappaB (NF-κB) induced by either 12-O-tetradecanoylphorbol 13-acetate (TPA) or ultraviolet-B (UVB). Extracts of all autumn olive genotypes inhibited proliferation of human leukemia HL-60 cancer cells and human lung epithelial cancer A549 cells and induced apoptosis of HL-60 cells. In particular, ‘Brilliant Rose’ and ‘Jewel’ had relatively potent activities compared to other genotypes. These results indicate that consuming autumn olive fruit may be beneficial to human health, although further studies are needed for confirmation.

Autumn olive - antioxidant capacity - antiproliferation - apoptotic cancer cells - Oleaster (Elaeagnaceae) - Elaeagnus umbellata Thunb.

References

• 1 Velioglu Y S, Mazza G, Gao L, Oomah B D. Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products.  J Agric Food Chem. 1998;  46 4113-7.
• 2 World Cancer Research Fund, American Institute for Cancer Research . Food, nutrition and the prevention of cancer: a global perspective. Washington; American Institute for Cancer Research 1997.
• 3 Ness A R, Powles J W. Fruit and vegetables, and cardiovascular disease: A review.  Int J Epidemiol. 1977;  26 1-13.
• 4 Dirr M A. Manual of woody landscape plants. Champaign; Stipes Publ. Co 1983.
• 5 Fordham I M, Clevidence BA,Wiley ER,Zimmerman R H. Fruit of autumn olive: A rich source of lycopene.  HortScience. 2001;  36 1136-7.
• 6 Foote C S, Denny R W. Chemistry of singlet oxygen. VII. Quenching by β-carotene.  J Am Chem Soc. 1968;  90 6233-5.
• 7 Burton G W, Ingold K U. β-Carotene: an unusual type of lipid antioxidant.  Science. 1984;  224 569-73.
• 8 Larson R A. The antioxidants of higher plants.  Phytochemistry. 1988;  27 969-78.
• 9 Pallett K E, Young A J. Carotenoids. In: Alscher RG, Hess JL, editors Antioxidants in higher plants. Boca Raton; CRC 1993: 71-4.
• 10 Krinsky N I. Actions of carotenoids in biological systems.  Annu Rev Nutr. 1993;  13 561-73.
• 11 Palozza P, Krinsky N I. Antioxidant effects of carotenoids in vitro and vivo: An overview.  Methods Enzymol. 1992;  213 403-20.
• 12 Le Marchand L, Murphy S P, Hankin J H, Wilkens L R, Kolonel L N. Flavonoid intake and lung cancer risk.  J Natl Cancer Inst. 2000;  92 154-60.
• 13 Nishino H. Cancer prevention by natural carotenoids. In: Packer L, Hiramatsu M, Yoshikawa T, editors Antioxidants food supplements in human health. New York; Academic Press 1999.
• 14 Mathews-Roth M M. Antitumor activity of beta-carotene, canthaxanthin and phytoene.  Oncology. 1982;  39 33-7.
• 15 Ukai N, Lu Y, Etoh H, Yagi A, Ina K, Oshima S. et al . Photosensitized oxygenation of lycopene.  Biosci Biotechnol Biochem. 1994;  58 1718-9.
• 16 Giovannucci E. Tomatoes, tomato-based products, lycopene and cancer: review of the epidemiological literature.  J Natl Cancer Inst. 1999;  91 317-31.
• 17 Olson J A. Carotenoids. In: Shils ME, Olson JA, Shik M, Ross AC, editors. Modern nutrition in health and disease. 9th edition.  Baltimore: Williams &. Wilkins;  1999 525-41.
• 18 Weisburger J H. Nutritional approach to cancer prevention with emphasis on vitamins, antioxidants and carotenoids.  Am J Clin Nutr. 1991;  53 226S-37S.
• 19 Bode A M, Dong Z. Signal transduction pathways: targets for chemoprevention of skin cancer.  Lancet Oncol. 2000;  1 181-8.
• 20 Baldwin AS J r. The NF-kappa B and I kappa B proteins: new discoveries and insights.  Annu Rev Immunol. 1996;  14 649-83.
• 21 Dong Z, Ma W, Huang C,Yang C S. Inhibition of tumor promoter-induced activator protein 1 activation and cell transformation by tea polyphenols, (-)-epigallocatechin gallate, and theaflavins.  Cancer Res. 1997;  57 414-9.
• 22 Hou D X, Kai K, Li J J, Lin S, Terahara N, Wakamatsu M. et al . Anthocyanidins inhibit activator protein 1 activity and cell transforation: structure-activity relationship and molecular mechanisms.  Carcinogenesis. 2004;  25 29-36.
• 23 Schulze-Osthoff K, Ferrari D, Riehemann K, Wesselborg S. Regulation of NF-kappa B activation by MAP kinase cascades.  Immunobiology. 1997;  198 35-49.
• 24 Li J J, Westergaard C, Ghosh P, Colburn N H. Inhibitors of both nuclear factor-kappaB and activator protein-1 activation block the neoplastic transformation response.  Cancer Res. 1997;  57 3569-6.
• 25 Leonard S S, Xia C, Jiang B H, Stinefelt B, Klandorf H, Harris G K. et al . Resveratrol scavenges reactive oxygen species and effects radical-induced cellular responses.  Biochem Biophys Res Commun. 2003;  309 1017-26.
• 26 Mosmann T. Rapid colorimetric assay for cellular growth and survival-application to proliferation and cyto-toxicity assays. J.  Immunol Methods. 1983;  65 55-63.
• 27 NCS S. Statistical analysis and graphics. Statistical software. Kaysville, Utah; 2007.
• 28 Muller J M, Rupec R A, Baeuerle P A. Study of gene regulation by NF-κB and AP-1 in response to reactive oxygen intermediates.  Methods. 1997;  11 301-13.
• 29 Huang C S, Ma W Y, Dawson M I, Rincon M, Flavell R A, Dong Z G. Blocking activator protein-1 activity, but not activating retinoic acid response element, is required for the antitumor promotion effect of retinoic acid.  Proc Natl Acad Sci USA. 1997;  94 5826-30.
• 30 Risse-Hackl G, Adamkiewicz J, Wimmel A, Schuermann M. Transition from SCLC to NSCLC phenotype is accompanied by an increased TRE-binding activity and recruitment of specific AP-1 proteins.  Oncogene. 1998;  16 3057-68.
• 31 Dumont J A, Bitonti A J, Wallace CD,Baumann R J, Cashman E A, Cross-Doersen D E. Progression of MCF-7 breast cancer cells to antiestrogen-resistant phenotype is accompanied by elevated levels of AP-1 DNA-binding activity.  Cell Growth Differ. 1996;  7 351-9.
• 32 Saez E, Rutberg S E, Mueller E, Oppenheim H, Smoluk J,Yuspa S H. et al . c-Fos is required for malignant progression of skin tumors.  Cell. 1995;  82 721-32.
• 33 Dong Z, Huang C, Brown R E, Ma W -Y. Inhibition of activator protein 1 activity and neoplastic transformation by aspirin.  J Biol Chem. 1997;  272 9962-70.
• 34 Hsu T, Young M R, Cmarik J, Colburn N H. Activator protein 1 (AP-1)- and nuclear factor κB (NF-κB)-dependent transcriptional events in carcinogenesis.  Free Radic Biol Med. 2000;  28 1338-48.
• 35 Evan G I, Vousden K H. Proliferation, cell cycle and apoptosis in cancer.  Nature. 2001;  411 342-8.
• 36 Kuntz S, Wenzel U, Daniel H. Comparative analysis of the effects of flavonoids on proliferation, cytotoxicity, and apoptosis in human colon cancer cell lines.  Eur J Nutr. 1999;  38 133-42.
• 37 Olsson M E, Gustavsson K, Andersson S, Nilsson Å, Duan R. Inhibition of cancer cell proliferation in vitro by fruit and berry extracts and correlations with antioxidant levels.  J Agric Food Chem. 2004;  52 7264-71.
• 38 Prakash P, Russel R M, Krinsky N I. In vitro inhibition of estrogen-dependent and estrogen-independent human breast cancer cells treated with carotenoids or retinoids.  J Nutr. 2001;  131 1574-80.
• 39 Wang S Y, Feng R, Bowman L, Penhallegon R, Ding M, Lu Y. Antioxidant activity in lingonberries (Vaccinium vitis-idaea L) and its inhibory effect on activator protein 1, nuclear factor-κB, and MAPK-activated protein kinases activation.  J Agric Food Chem. 2005;  53 3156-66.
• 40 Xue H, Aziz R M, Sun N, Cassady J M, Kamendulis L M, Xu Y. et al . Inhibition of cellular transformation by berry extracts.  Carcinogenesis (Lond.). 2001;  22 351-6.