Research Article: Identification of 3-hydroxy-β-damascone and related carotenoid-derived aroma compounds as novel potent inducers of Nrf2-mediated phase 2 response with concomitant anti-inflammatory activity

Molecular Nutrition and Food Research

Volumn 53, Issue 10, 2009, Pages 1237-1244

  Gerhäuser, Clarissa ^a   Klimo, Karin ^a   Hümmer, Wolfgang ^b   Hölzer, Jana ^c   Petermann, Astrid ^c   Garreta Rufas, Antonio ^a   Böhmer, Frank D ^c   Schreier, Peter ^b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Apple juice; Apples; Cancer chemoprevention; Carotenoid derived aroma compounds; NAD(P)H:quinone oxidoreductase

Indexed keywords

ANIMALIA; MALUS X DOMESTICA;

3 HYDROXY BETA DAMASCONE; 3-HYDROXY-BETA-DAMASCONE; ANTINEOPLASTIC AGENT; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; NONSTEROID ANTIINFLAMMATORY AGENT; NORISOPRENOID; NQO1 PROTEIN, MOUSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); TRANSCRIPTION FACTOR NRF2; VOLATILE ORGANIC COMPOUND;

ANIMAL; APPLE; ARTICLE; CELL LINE; CELL SURVIVAL; CHEMISTRY; DRUG ANTAGONISM; DRUG DETOXIFICATION; FRUIT; GENETICS; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTICARCINOGENIC AGENTS; CELL LINE; CELL SURVIVAL; FRUIT; HUMANS; LIPOPOLYSACCHARIDES; MALUS; METABOLIC DETOXICATION, PHASE II; MICE; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; NITRIC OXIDE SYNTHASE TYPE II; NORISOPRENOIDS; VOLATILE ORGANIC COMPOUNDS;

EID: 70350060460     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200800492     Document Type: Article

References (44)

1. AICR, Food, Nutrition, Physical Activity, and the Prevention of Cancer: A Global Perspective, AICR, Washington, DC 2007.
2. Ellinger, W., ZMP-Marktbilanz Obst 2007, Deutschland Europ ische Union Weltmarkt, ZMP Zentrale Marktund Preisberichtstelle GmbH, Bonn 2007.
3. Gerhauser, C., Cancer chemopreventive potential of apples, apple juice, and apple components, Planta Med. 2008, 74, 1608-1624.
4. Zessner, H., Pan, L., Will, F., Klimo, K., et al., Fractionation of polyphenol-enriched apple juice extracts to identify constituents with cancer chemopreventive potential, Mol. Nutr. Food Res. 2008, 52, S28-S44.
5. Kohle, C., Bock, K. W., Coordinate regulation of Phase I and II xenobiotic metabolisms by the Ah receptor and Nrf2, Bio-chem. Pharmacol. 2007, 73, 1853-1862.
6. Eggler, A. L., Gay, K. A., Mesecar, A. D., Molecular mechanisms of natural products in chemoprevention: Induction of cytoprotective enzymes by Nrf2, Mol. Nutr. Food Res. 2008, 52 (Suppl. 1), S84-94.
7. Hayes, J. D., McMahon, M., Molecular basis for the contribution of the antioxidant responsive element to cancer chemoprevention, Cancer Lett. 2001, 174, 103-113.
8. McMahon, M., Itoh, K., Yamamoto, M., Chanas, S. A., et al., The Cap̀n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes, Cancer Res. 2001, 61, 3299-3307.
9. Dinkova-Kostova, A. T., Fahey, J. W., Talalay, P., Chemical structures of inducers of nicotinamide quinone oxidoreductase 1 (NQO1), Methods Enzymol. 2004, 382, 423-448.
10. Kang, Y. H., Pezzuto, J. M., Induction of quinone reductase as a primary screen for natural product anticarcinogens, Methods Enzymol. 2004, 382, 380-414.
11. Surburg, H., Panten, I., Common Fragrance and Flavor Materials, Wiley VCH, Weinheim 2006.
12. Gerhauser, C., Heiss, E., Herhaus, C., Klimo, K., in: Johnson, I. T., Fenwick, G. R. (Eds.), Dietary Anticarcinogens and Antimutagens: Chemical and Biological Aspects, Royal Society of Chemistry, Cambridge 2001, pp. 189-192.
13. Heiss, E., Herhaus, C., Klimo, K., Bartsch, H., Gerhauser, C., Nuclear factor kappa B is a molecular target for sulforaphane-mediated anti-inflammatory mechanisms, J. Biol. Chem. 2001, 276, 32008-32015.
14. Liu, H., Dinkova-Kostova, A. T., Talalay, P., Coordinate regulation of enzyme markers for inflammation and for protection against oxidants and electrophiles, Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 15926-15931.
15. Schoch, E., Benda, I., Schreier, P., Bioconversion of alpha- Damascone by Botrytis cinerea, Appl. Environ. Microbiol. 1991,57,15-18.
16. Winterhalter, P., 1,1,6-Trimethyl-1,2-dihydronaphthalene (Tdn) formation in wine 1. Studies on the hydrolysis of 2,6,10,10-tetramethyl-1-oxaspiro[4.5]dec-6-ene-2,8-diol rationalizing the origin of Tdn and related C-13 norisoprenoids in Riesling wine, J. Agric. Food Chem. 1991, 39, 1825-1829.
17. Herderich, M., Doctoral thesis, University of W rzburg, Germany 1992.
18. Gerhauser, C., You, M., Liu, J., Moriarty, R. M., et al., Cancer chemopreventive potential of sulforamate, a novel analogue of sulforaphane that induces phase 2 drug-metabolizing enzymes, Cancer Res. 1997, 57, 272-278.
19. Skehan, P., Storeng, R., Scudiero, D., Monks, A., et al., New colorimetric cytotoxicity assay for anticancer-drug screening, J. Natl. Cancer Inst. 1990, 82, 1107-1112.
20. Kobayashi, A., Kang, M. I., Watai, Y., Tong, K. I., et al., Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1, Mol. Cell. Biol. 2006,26,221-229.
21. Dyer, B. W., Ferrer, F. A., Klinedinst, D. K., Rodriguez, R., A noncommercial dual luciferase enzyme assay system for reporter gene analysis, Anal. Biochem. 2000, 282, 158-161.
22. Fuhrmann, E., Grosch, W., Character impact odorants of the apple cultivars Elstar and Cox Orange, Nahrung 2002, 46, 187-193.
23. Osburn, W. O., Kensler, T. W., Nrf2 signaling: An adaptive response pathway for protection against environmental toxic insults, Mutat. Res. 2008, 659, 31-39.
24. Gomes-Carneiro, M. R., Dias, D. M. M., Paumgartten, F. J. R., Study on the mutagenicity and antimutagenicity of betaionone in the Salmonella/microsome assay, Food Chem. Toxicol. 2006, 44, 522-527.
25. De-Oliveira, A. C. A. X., Fidalgo-Neto, A. A., Paumgartten, F. J. R., In vitro inhibition of liver monooxygenases by betaionone, 1,8-cineole, (-)menthol and terpineol, Toxicology 1999,135,33-41.
26. Jeong, T. C., Kim, H. J., Yun, C. H., Lee, S. S., et al., Induction of liver cytochrome-P450 2b1 by beta-ionone in Sprague-Dawley rats, Biochem. Biophys. Res. Commun. 1995,216,198-202.
27. Duncan, R. E., Lau, D., El-Sohemy, A., Archer, M. C., Geraniol and beta-ionone inhibit proliferation, cell cycle progression, and cyclin-dependent kinase 2 activity in MCF-7 breast cancer cells independent of effects on HMG-CoA reductase activity, Biochem. Pharmacol. 2004, 68, 1739-1747.
28. Liu, J. R., Yang, B. F., Chen, B. Q., Yang, Y. M., et al., Inhibition of beta-ionone on SGC-7901 cell proliferation and upregulation of metalloproteinases-1 and -2 expression, World J. Gastroenterol. 2004, 10, 167-171.
29. Janakiram, N. B., Cooma, I., Mohammed, A., Steele, V. E., Rao, C. V., b-Ionone inhibits colonic aberrant crypt foci formation in rats, suppresses cell growth, and induces retinoid X receptor-alpha in human colon cancer cells, Mol. Cancer Ther. 2008, 7, 181-190.
30. Yu, S. G., Anderson, P. J., Elson, C. E., Efficacy of b-ionone in the chemoprevention of rat mammary carcinogenesis, J. Agric. Food Chem. 1995, 43, 2144-2147.
31. Liu, J. R., Sun, X. R., Dong, H. W., Sun, C. H., et al., b-Ionone suppresses mammary carcinogenesis, proliferative activity and induces apoptosis in the mammary gland of the Sprague-Dawley rat, Int. J. Cancer 2008, 122, 2689-2698.
32. Pongprayoon, U., Baeckstrom, P., Jacobsson, U., Lindstrom, M., Bohlin, L., Antispasmodic activity of beta-damascenone and E-phytol isolated from Ipomoea pes-caprae, Planta Med. 1992,58,19-21.
33. Becherel, P. A., Chosidow, O., Le Goff, L., Frances, C., et al., Inducible nitric oxide synthase and proinflammatory cytokine expression by human keratinocytes during acute urticaria, Mol. Med. 1997, 3, 686-694.
34. Ross, R., Gillitzer, C., Kleinz, R., Schwing, J., et al., Involvement of NO in contact hypersensitivity, Int. Immunol. 1998, 10,61-69.
35. Dinkova-Kostova, A. T., Massiah, M. A., Bozak, R. E., Hicks, R. J., Talalay, P., Potency of Michael reaction acceptors as inducers of enzymes that protect against carcinogenesis depends on their reactivity with sulfhydryl groups, Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 3404-3409.
36. Prestera, T., Talalay, P., Alam, J., Ahn, Y. I., et al., Parallel induction of heme oxygenase-1 and chemoprotective phase 2 enzymes by electrophiles and antioxidants: Regulation by upstream antioxidant-responsive elements (ARE), Mol. Med. 1995,1,827-837.
37. Otterbein, L. E., Bach, F. H., Alam, J., Soares, M., et al., Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway, Nat. Med. 2000, 6, 422-428.
38. Ashino, T., Yamanaka, R., Yamamoto, M., Shimokawa, H., et al., Negative feedback regulation of lipopolysaccharide-induced inducible nitric oxide synthase gene expression by heme oxygenase-1 induction in macrophages, Mol. Immunol. 2008,45,2106-2115.
39. Lee, T. S., Tsai, H. L., Chau, L. Y., Induction of heme oxygen- ase-1 expression in murine macrophages is essential for the anti-inflammatory effect of low dose 15-deoxy-Delta 12,14- prostaglandin J2, J. Biol. Chem. 2003, 278, 19325-19330.
40. Lin, H. Y., Juan, S. H., Shen, S. C., Hsu, F. L., Chen, Y. C., Inhibition of lipopolysaccharide-induced nitric oxide production by flavonoids in RAW264.7 macrophages involves heme oxygenase-1, Biochem. Pharmacol. 2003, 66, 1821-1832.
41. Abuarqoub, H., Foresti, R., Green, C. J., Motterlini, R., Heme oxygenase-1 mediates the anti-inflammatory actions of 29- hydroxychalcone in RAW 264.7 murine macrophages, Am. J. Physiol., Cell Physiol. 2006, 290, C1092-C1099.
42. Kim, B. C., Choi, J. W., Hong, H. Y., Lee, S. A., et al., Heme oxygenase-1 mediates the anti-inflammatory effect of mushroom Phellinus linteus in LPS-stimulated RAW264.7 macrophages, J. Ethnopharmacol. 2006, 106, 364-371.
43. Jeon, W. K., Kim, B. C., Heme oxygenase-1 mediates the anti-inflammatory effect of propyl gallate in LPS-stimulated macrophages, Biochem. Biophys. Res. Commun. 2007, DOI: 10.1016/j.bbrc.2007.07.056.
44. Kim, K. M., Pae, H. O., Zhung, M., Ha, H. Y., et al., Involvement of anti-inflammatory heme oxygenase-1 in the inhibitory effect of curcumin on the expression of pro-inflammatory inducible nitric oxide synthase in RAW264.7 macrophages, Biomed. Pharmacother. 2008, 62, 630-636.