Characterization of thiol-conjugated metabolites of ginger components shogaols in mouse and human urine and modulation of the glutathione levels in cancer cells by [6]-shogaol

Molecular Nutrition and Food Research

Volumn 57, Issue 3, 2013, Pages 447-458

  Chen, Huadong ^a   Soroka, Dominique N ^a   Hu, Yuhui ^b   Chen, Xiaoxin ^b   Sang, Shengmin ^a  

^a NORTH CAROLINA A AND T STATE UNIVERSITY   (United States)

^b NORTH CAROLINA CENTRAL UNIVERSITY   (United States)

Author keywords

Glutathione; Human urine; Shogaols; Thiol conjugated metabolites

Indexed keywords

(10) SHOGAOL; (10)-SHOGAOL; (8) SHOGAOL; (8)-SHOGAOL; ACETYLCYSTEINE; ANTINEOPLASTIC AGENT; CATECHOL DERIVATIVE; DRUG DERIVATIVE; GLUTATHIONE; GUAIACOL; SHOGAOL; THIOL DERIVATIVE;

ADULT; ANIMAL; ARTICLE; BEVERAGE; C57BL MOUSE; CELL STRAIN HCT116; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; FEMALE; GINGER; HUMAN; MALE; METABOLISM; MOUSE; TANDEM MASS SPECTROMETRY; TUMOR CELL LINE; URINE;

ACETYLCYSTEINE; ADULT; ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; BEVERAGES; CATECHOLS; CELL LINE, TUMOR; FEMALE; GINGER; GLUTATHIONE; GUAIACOL; HCT116 CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MOLECULAR STRUCTURE; SULFHYDRYL COMPOUNDS; TANDEM MASS SPECTROMETRY;

MUS; ZINGIBER OFFICINALE;

EID: 84875052345     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200679     Document Type: Article

References (37)

1. Nakamura, Y., Miyoshi, N., Electrophiles in foods: the current status of isothiocyanates and their chemical biology. Biosci. Biotechnol. Biochem. 2010, 74, 242-255.
2. Leung, A. Y., Foster, S., Encyclopedia of Common Natural Ingredients used in Food, Drugs and Cosmetics, 2nd Edn. Wiley, New York 1996, p. 271-274.
3. Jiang, H., Solyom, A. M., Timmermann, B. N., Gang, D. R., Characterization of gingerol-related compounds in ginger rhizome (Zingiber officinale Rosc.) by high-performance liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom. 2005, 19, 2957-2964.
4. Jiang, H., Timmermann, B. N., Gang, D. R., Characterization and identification of diarylheptanoids in ginger (Zingiber officinale Rosc.) using high-performance liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom. 2007, 21, 509-518.
5. Jiang, H., Xie, Z., Koo, H. J., McLaughlin, S. P. et al., Metabolic profiling and phylogenetic analysis of medicinal Zingiber species: tools for authentication of ginger (Zingiber officinale Rosc.). Phytochemistry 2006, 67, 1673-1685.
6. Yu, Y., Huang, T., Yang, B., Liu, X. et al., Development of gas chromatography-mass spectrometry with microwave distillation and simultaneous solid-phase microextraction for rapid determination of volatile constituents in ginger. J. Pharm. Biomed. Anal. 2007, 43, 24-31.
7. Masada, Y., Inoue, T., Hashimoto, K., Fujioka, M. et al., Studies on the constituents of ginger (Zingiber officinale Roscoe) by GC-MS (author's transl). Yakugaku Zasshi 1974, 94, 735-738.
8. Chen, C. Y., Liu, T. Z., Liu, Y. W., Tseng, W. C. et al., 6-Shogaol (alkanone from ginger) induces apoptotic cell death of human hepatoma p53 mutant Mahlavu subline via an oxidative stress-mediated caspase-dependent mechanism. J. Agric. Food Chem. 2007, 55, 948-954.
9. Pan, M. H., Hsieh, M. C., Hsu, P. C., Ho, S. Y. et al., 6-Shogaol suppressed lipopolysaccharide-induced up-expression of iNOS and COX-2 in murine macrophages. Mol. Nutr. Food Res. 2008, 52, 1467-1477.
10. Gan, F. F., Nagle, A. A., Ang, X., Ho, O. H. et al., Shogaols at proapoptotic concentrations induce G(2)/M arrest and aberrant mitotic cell death associated with tubulin aggregation. Apoptosis 2011, 16, 856-867.
11. Ling, H., Yang, H., Tan, S. H., Chui, W. K. et al., 6-Shogaol, an active constituent of ginger, inhibits breast cancer cell invasion by reducing matrix metalloproteinase-9 expression via blockade of nuclear factor-kappaB activation. Br. J. Pharmacol. 2010, 161, 1763-1777.
12. Hu, R., Zhou, P., Peng, Y. B., Xu, X. et al., 6-Shogaol induces apoptosis in human hepatocellular carcinoma cells and exhibits anti-tumor activity in vivo through endoplasmic reticulum stress. PLoS One 2012, 7, e39664.
13. Sang, S., Hong, J., Wu, H., Liu, J. et al., Increased growth inhibitory effects on human cancer cells and anti-inflammatory potency of shogaols from Zingiber officinale relative to gingerols. J. Agric. Food Chem. 2009, 57, 10645-10650.
14. Chen, H., Lv, L., Soroka, D., Warin, R. F. et al., Metabolism of [6]-shogaol in mice and in cancer cells. Drug Metab. Dispos. 2012, 40, 742-753.
15. Iwabu, J., Watanabe, J., Hirakura, K., Ozaki, Y. et al., Profiling of the compounds absorbed in human plasma and urine after oral administration of a traditional Japanese (kampo) medicine, daikenchuto. Drug Metab. Dispos. 2010, 38, 2040-2048.
16. Wang, W., Li, C. Y., Wen, X. D., Li, P. et al., Simultaneous determination of 6-gingerol, 8-gingerol, 10-gingerol and 6-shogaol in rat plasma by liquid chromatography-mass spectrometry: application to pharmacokinetics. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2009, 877, 671-679.
17. Zick, S. M., Djuric, Z., Ruffin, M. T., Litzinger, A. J. et al., Pharmacokinetics of 6-gingerol, 8-gingerol, 10-gingerol, and 6-shogaol and conjugate metabolites in healthy human subjects. Cancer Epidemiol. Biomarkers Prev. 2008, 17, 1930-1936.
18. Zick, S. M., Ruffin, M. T., Djuric, Z., Normolle, D. et al., Quantitation of 6-, 8- and 10-gingerols and 6-shogaol in human plasma by high-performance liquid chromatography with electrochemical detection. Int. J. Biomed. Sci. 2010, 6, 233-240.
19. Asami, A., Shimada, T., Mizuhara, Y., Asano, T. et al., Pharmacokinetics of [6]-shogaol, a pungent ingredient of Zingiber officinale Roscoe (Part I). J. Nat. Med. 2010, 64, 281-287.
20. Yu, Y., Zick, S., Li, X., Zou, P. et al., Examination of the pharmacokinetics of active ingredients of ginger in humans. AAPS J. 2011, 13, 417-426.
21. Falletti, O., Cadet, J., Favier, A., Douki, T., Trapping of 4-hydroxynonenal by glutathione efficiently prevents formation of DNA adducts in human cells. Free Radic. Biol. Med. 2007, 42, 1258-1269.
22. Hayes, J. D., McLellan, L. I., Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic. Res. 1999, 31, 273-300.
23. Rudd, L. P., Kabler, S. L., Morrow, C. S., Townsend, A. J., Enhanced glutathione depletion, protein adduct formation, and cytotoxicity following exposure to 4-hydroxy-2-nonenal (HNE) in cells expressing human multidrug resistance protein-1 (MRP1) together with human glutathione S-transferase-M1 (GSTM1). Chem. Biol. Interact. 2011, 194, 113-119.
24. Ahn, Y. H., Hwang, Y., Liu, H., Wang, X. J. et al., Electrophilic tuning of the chemoprotective natural product sulforaphane. Proc. Natl. Acad. Sci. USA 2011, 107, 9590-9595.
25. Kassahun, K., Davis, M., Hu, P., Martin, B. et al., Biotransformation of the naturally occurring isothiocyanate sulforaphane in the rat: identification of phase I metabolites and glutathione conjugates. Chem. Res. Toxicol. 1997, 10, 1228-1233.
26. Pernice, R., Hauder, J., Koehler, P., Vitaglione, P. et al., Effect of sulforaphane on glutathione-adduct formation and on glutathione_S_transferase-dependent detoxification of acrylamide in Caco-2 cells. Mol. Nutr. Food Res. 2009, 53, 1540-1550.
27. Lipnick, R. L., Outliers - their origin and use in the classification of molecular mechanisms of toxicity. Sci. Total Environ. 1991, 109, 131-153.
28. Ishiguro, K., Ando, T., Watanabe, O., Goto, H., Specific reaction of alpha, beta-unsaturated carbonyl compounds such as 6-shogaol with sulfhydryl groups in tubulin leading to microtubule damage. FEBS Lett. 2008, 582, 3531-3536.
29. Hayes, J. D., McMahon, M., Chowdhry, S., Dinkova-Kostova, A. T., Cancer chemoprevention mechanisms mediated through the Keap1-Nrf2 pathway. Antioxid. Redox. Signal 2010, 13, 1713-1748.
30. Bak, M. J., Ok, S., Jun, M., Jeong, W. S., 6-Shogaol-rich extract from ginger up-regulates the antioxidant defense systems in cells and mice. Molecules 2012, 17, 8037-8055.
31. Luo, Y., Eggler, A. L., Liu, D., Liu, G. et al., Sites of alkylation of human Keap1 by natural chemoprevention agents. J. Am. Soc. Mass Spectrom. 2007, 18, 2226-2232.
32. Shao, X., Lv, L., Parks, T., Wu, H. et al., Quantitative analysis of ginger components in commercial products using liquid chromatography with electrochemical array detection. J. Agric. Food Chem. 2010, 58, 12608-12614.
33. Shao, X., Chen, X., Badmaev, V., Ho, C. T. et al., Structural identification of mouse urinary metabolites of pterostilbene using liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2010, 24, 1770-1778.
34. Kensler, T. W., Chemoprevention by inducers of carcinogen detoxication enzymes. Environ. Health Perspect. 1997, 105(Suppl 4), 965-970.
35. Juge, N., Mithen, R. F., Traka, M., Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cell Mol. Life Sci. 2007, 64, 1105-1127.
36. Higgins, L. G., Kelleher, M. O., Eggleston, I. M., Itoh, K. et al., Transcription factor Nrf2 mediates an adaptive response to sulforaphane that protects fibroblasts in vitro against the cytotoxic effects of electrophiles, peroxides and redox-cycling agents. Toxicol. Appl. Pharmacol. 2009, 237, 267-280.
37. MacLeod, A. K., McMahon, M., Plummer, S. M., Higgins, L. G. et al., Characterization of the cancer chemopreventive NRF2-dependent gene battery in human keratinocytes: demonstration that the KEAP1-NRF2 pathway, and not the BACH1-NRF2 pathway, controls cytoprotection against electrophiles as well as redox-cycling compounds. Carcinogenesis 2009, 30, 1571-1580.