Dietary catechins and procyanidins modulate zinc homeostasis in human HepG2 cells

Journal of Nutritional Biochemistry

Volumn 22, Issue 2, 2011, Pages 153-163

  Quesada, Isabel M ^a   Bustos, Mario ^a   Blay, Mayte ^a   Pujadas, Gerard ^a   Ardèvol, Anna ^a   Salvadó, M Josepa ^a   Bladé, Cinta ^a   Arola, Lluís ^a   Fernández Larrea, Juan ^a  

^a UNIVERSITAT ROVIRA I VIRGILI   (Spain)

Author keywords

Epigallocatechin gallate; Flavonoids; Labile zinc; Metallothionein; Procyanidins; Zinc transporters

Indexed keywords

CATECHIN; CHELATING AGENT; EPIGALLOCATECHIN GALLATE; GRAPE SEED EXTRACT; GREEN TEA EXTRACT; INTERLEUKIN 6; LACTATE DEHYDROGENASE; MESSENGER RNA; PROCYANIDIN; SODIUM PHOSPHATE COTRANSPORTER 2A; ZINC;

ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; CANCER CELL CULTURE; CELL METABOLISM; CONTROLLED STUDY; FLUORESCENCE; HOMEOSTASIS; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

BIFLAVONOIDS; CARCINOMA, HEPATOCELLULAR; CATECHIN; CATION TRANSPORT PROTEINS; DIET; GENE EXPRESSION REGULATION; GRAPE SEED EXTRACT; HEP G2 CELLS; HOMEOSTASIS; HUMANS; INTERLEUKIN-6; LIVER NEOPLASMS; METALLOTHIONEIN; PROANTHOCYANIDINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TEA; ZINC;

VITACEAE;

EID: 78651245880     PISSN: 09552863     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2009.12.009     Document Type: Article

References (62)

1. Rasmussen S.E., Frederiksen H., Struntze Krogholm K., Poulsen L. Dietary proanthocyanidins: occurrence, dietary intake, bioavailability, and protection against cardiovascular disease. Mol Nutr Food Res 2005, 49:159-174.
2. Aron P.M., Kennedy J.A. Flavan-3-ols: nature, occurrence and biological activity. Mol Nutr Food Res 2008, 52:79-104.
3. Stangl V., Dreger H., Stangl K., Lorenz M. Molecular targets of tea polyphenols in the cardiovascular system. Cardiovasc Res 2007, 73:348-358.
4. Del Bas J.M., Fernandez-Larrea J., Blay M., Ardevol A., Salvado M.J., Arola L., et al. Grape seed procyanidins improve atherosclerotic risk index and induce liver CYP7A1 and SHP expression in healthy rats. Faseb J 2005, 19:479-481.
5. Montagut G., Onnockx S., Vaque M., Blade C., Blay M., Fernandez-Larrea J., et al. Oligomers of grape-seed procyanidin extract activate the insulin receptor and key targets of the insulin signaling pathway differently from insulin. J Nutr Biochem 2009, [Epub ahead of press; doi:10.1016/j.jnutbio.2009.02.003].
6. Mackenzie G.G., Carrasquedo F., Delfino J.M., Keen C.L., Fraga C.G., Oteiza P.I. Epicatechin, catechin, and dimeric procyanidins inhibit PMA-induced NF-kappaB activation at multiple steps in Jurkat T cells. Faseb J 2004, 18:167-169.
7. Terra X., Valls J., Vitrac X., Merrillon J.M., Arola L., Ardevol A., et al. Grape-seed procyanidins act as antiinflammatory agents in endotoxin-stimulated RAW 264.7 macrophages by inhibiting NFkB signaling pathway. J Agric Food Chem 2007, 55:4357-4365.
8. Scalbert A., Mila I., Expert D., Marmolle F., Albrecht A.M., Hurrell R., et al. Polyphenols, metal ion complexation and biological consequences. Basic Life Sci 1999, 66:545-554.
9. Hider R.C., Liu Z.D., Khodr H.H. Metal chelation of polyphenols. Methods Enzymol 2001, 335:190-203.
10. Na H.K., Surh Y.J. Intracellular signaling network as a prime chemopreventive target of (-)-epigallocatechin gallate. Mol Nutr Food Res 2006, 50:152-159.
11. Na H.K., Surh Y.J. Modulation of Nrf2-mediated antioxidant and detoxifying enzyme induction by the green tea polyphenol EGCG. Food Chem Toxicol 2008, 46:1271-1278.
12. Puiggros F., Llopiz N., Ardevol A., Blade C., Arola L., Salvado M.J. Grape seed procyanidins prevent oxidative injury by modulating the expression of antioxidant enzyme systems. J Agric Food Chem 2005, 53:6080-6086.
13. Williams R.J., Spencer J.P., Rice-Evans C. Flavonoids: antioxidants or signalling molecules?. Free Radic Biol Med 2004, 36:838-849.
14. Scalbert A., Johnson I.T., Saltmarsh M. Polyphenols: antioxidants and beyond. Am J Clin Nutr 2005, 81:215S-217S.
15. Peluso M.R. Flavonoids attenuate cardiovascular disease, inhibit phosphodiesterase, and modulate lipid homeostasis in adipose tissue and liver. Exp Biol Med (Maywood) 2006, 231:1287-1299.
16. Khan N., Mukhtar H. Multitargeted therapy of cancer by green tea polyphenols. Cancer Lett 2008, 269:269-280.
17. Kagaya N., Kawase M., Maeda H., Tagawa Y., Nagashima H., Ohmori H., et al. Enhancing effect of zinc on hepatoprotectivity of epigallocatechin gallate in isolated rat hepatocytes. Biol Pharm Bull 2002, 25:1156-1160.
18. Sun S.L., He G.Q., Yu H.N., Yang J.G., Borthakur D., Zhang L.C., et al. Free Zn(2+) enhances inhibitory effects of EGCG on the growth of PC-3 cells. Mol Nutr Food Res 2008, 52:465-471.
19. Esparza I., Salinas I., Santamaría C., García-Mina J.M., Fernández J.M. Electrochemical and theoretical complexation studies for Zn and Cu with individual polyphenols. Analytica Chimica Acta 2005, 543:267-274.
20. Daniel H., tom Dieck H. Nutrient-gene interactions: a single nutrient and hundreds of target genes. Biol Chem 2004, 385:571-583.
21. tom Dieck H., Doring F., Fuchs D., Roth H.P., Daniel H. Transcriptome and proteome analysis identifies the pathways that increase hepatic lipid accumulation in zinc-deficient rats. J Nutr 2005, 135:199-205.
22. Coyle P., Zalewski P.D., Philcox J.C., Forbes I.J., Ward A.D., Lincoln S.F., et al. Measurement of zinc in hepatocytes by using a fluorescent probe, zinquin: relationship to metallothionein and intracellular zinc. Biochem J 1994, 303:781-786.
23. Beyersmann D., Haase H. Functions of zinc in signaling, proliferation and differentiation of mammalian cells. Biometals 2001, 14:331-341.
24. Murakami M., Hirano T. Intracellular zinc homeostasis and zinc signaling. Cancer Sci 2008, 99:1515-1522.
25. Hirano T., Murakami M., Fukada T., Nishida K., Yamasaki S., Suzuki T. Roles of zinc and zinc signaling in immunity: zinc as an intracellular signaling molecule. Adv Immunol 2008, 97:149-176.
26. Maret W. Molecular aspects of human cellular zinc homeostasis: redox control of zinc potentials and zinc signals. Biometals 2009, 22:149-157.
27. Cousins R.J., Liuzzi J.P., Lichten L.A. Mammalian zinc transport, trafficking, and signals. J Biol Chem 2006, 281:24085-24089.
28. Eide D.J. Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta 2006, 1763:711-722.
29. Sekler I., Sensi S.L., Hershfinkel M., Silverman W.F. Mechanism and regulation of cellular zinc transport. Mol Med 2007, 13:337-343.
30. Krezel A., Hao Q., Maret W. The zinc/thiolate redox biochemistry of metallothionein and the control of zinc ion fluctuations in cell signaling. Arch Biochem Biophys 2007, 463:188-200.
31. Krezel A., Maret W. Thionein/metallothionein control Zn(II) availability and the activity of enzymes. J Biol Inorg Chem 2008, 13:401-409.
32. Coyle P., Philcox J.C., Carey L.C., Rofe A.M. Metallothionein: the multipurpose protein. Cell Mol Life Sci 2002, 59:627-647.
33. Haq F., Mahoney M., Koropatnick J. Signaling events for metallothionein induction. Mutat Res 2003, 533:211-226.
34. Laity J.H., Andrews G.K. Understanding the mechanisms of zinc-sensing by metal-response element binding transcription factor-1 (MTF-1). Arch Biochem Biophys 2007, 463:201-210.
35. Devirgiliis C., Zalewski P.D., Perozzi G., Murgia C. Zinc fluxes and zinc transporter genes in chronic diseases. Mutat Res 2007, 622:84-93.
36. Mocchegiani E., Giacconi R., Malavolta M. Zinc signalling and subcellular distribution: emerging targets in type 2 diabetes. Trends Mol Med 2008, 14:419-428.
37. Hogstrand C., Kille P., Nicholson R.I., Taylor K.M. Zinc transporters and cancer: a potential role for ZIP7 as a hub for tyrosine kinase activation. Trends Mol Med 2009, 15:101-111.
38. Kuo S.M., Leavitt P.S., Lin C.P. Dietary flavonoids interact with trace metals and affect metallothionein level in human intestinal cells. Biol Trace Elem Res 1998, 62:135-153.
39. Kuo S.M., Leavitt P.S. Genistein increases metallothionein expression in human intestinal cells, Caco-2. Biochem Cell Biol 1999, 77:79-88.
40. Kuo S.M., Huang C.T., Blum P., Chang C. Quercetin cumulatively enhances copper induction of metallothionein in intestinal cells. Biol Trace Elem Res 2001, 84:1-10.
41. Gao Z., Xu H., Chen X., Chen H. Antioxidant status and mineral contents in tissues of rutin and baicalin fed rats. Life Sci 2003, 73:1599-1607.
42. Uchiyama S., Yamaguchi M. Genistein and zinc synergistically stimulate apoptotic cell death and suppress RANKL signaling-related gene expression in osteoclastic cells. J Cell Biochem 2007, 101:529-542.
43. Devergnas S., Chimienti F., Naud N., Pennequin A., Coquerel Y., Chantegrel J., et al. Differential regulation of zinc efflux transporters ZnT-1, ZnT-5 and ZnT-7 gene expression by zinc levels: a real-time RT-PCR study. Biochem Pharmacol 2004, 68:699-709.
44. Reaves S.K., Fanzo J.C., Arima K., Wu J.Y., Wang Y.R., Lei K.Y. Expression of the p53 tumor suppressor gene is up-regulated by depletion of intracellular zinc in HepG2 cells. J Nutr 2000, 130:1688-1694.
45. Zalewski P., Truong-Tran A., Lincoln S., Ward D., Shankar A., Coyle P., et al. Use of a zinc fluorophore to measure labile pools of zinc in body fluids and cell-conditioned media. Biotechniques 2006, 40:509-520.
46. Cao J., Bobo J.A., Liuzzi J.P., Cousins R.J. Effects of intracellular zinc depletion on metallothionein and ZIP2 transporter expression and apoptosis. J Leukoc Biol 2001, 70:559-566.
47. Shen H., Qin H., Guo J. Cooperation of metallothionein and zinc transporters for regulating zinc homeostasis in human intestinal Caco-2 cells. Nutr Res 2008, 28:406-413.
48. Cousins R.J., Blanchard R.K., Moore J.B., Cui L., Green C.L., Liuzzi J.P., et al. Regulation of zinc metabolism and genomic outcomes. J Nutr 2003, 133:1521S-1526S.
49. Langmade S.J., Ravindra R., Daniels P.J., Andrews G.K. The transcription factor MTF-1 mediates metal regulation of the mouse ZnT1 gene. J Biol Chem 2000, 275:34803-34809.
50. Liuzzi J.P., Lichten L.A., Rivera S., Blanchard R.K., Aydemir T.B., Knutson M.D., et al. Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proc Natl Acad Sci U S A 2005, 102:6843-6848.
51. Serra A., Macia A., Romero M.P., Salvado M.J., Bustos M., Fernandez-Larrea J., et al. Determination of procyanidins and their metabolites in plasma samples by improved liquid chromatography-tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 2009, 877:1169-1176.
52. Shoji T., Masumoto S., Moriichi N., Akiyama H., Kanda T., Ohtake Y., et al. Apple procyanidin oligomers absorption in rats after oral administration: analysis of procyanidins in plasma using the porter method and high-performance liquid chromatography/tandem mass spectrometry. J Agric Food Chem 2006, 54:884-892.
53. Chow H.H., Cai Y., Alberts D.S., Hakim I., Dorr R., Shahi F., et al. Phase I pharmacokinetic study of tea polyphenols following single-dose administration of epigallocatechin gallate and polyphenon E. Cancer Epidemiol Biomarkers Prev 2001, 10:53-58.
54. Quesada I.M., Del Bas J.M., Blade C., Ardevol A., Blay M., Salvado M.J., et al. Grape seed procyanidins inhibit the expression of metallothionein genes in human HepG2 cells. Genes Nutr 2007, 2:105-109.
55. Wren A.F., Cleary M., Frantz C., Melton S., Norris L. 90-day oral toxicity study of a grape seed extract (IH636) in rats. J Agric Food Chem 2002, 50:2180-2192.
56. Chung M.J., Kang A.Y., Lee K.M., Oh E., Jun H.J., Kim S.Y., et al. Water-soluble genistin glycoside isoflavones up-regulate antioxidant metallothionein expression and scavenge free radicals. J Agric Food Chem 2006, 54:3819-3826.
57. Zhang J.J., Wu M., Schoene N.W., Cheng W.H., Wang T.T., Alshatwi A.A., et al. Effect of resveratrol and zinc on intracellular zinc status in normal human prostate epithelial cells. Am J Physiol Cell Physiol 2009, 297:C632-C644.
58. Shamim U., Hanif S., Ullah M.F., Azmi A.S., Bhat S.H., Hadi S.M. Plant polyphenols mobilize nuclear copper in human peripheral lymphocytes leading to oxidatively generated DNA breakage: implications for an anticancer mechanism. Free Radic Res 2008, 42:764-772.
59. Datta J., Majumder S., Kutay H., Motiwala T., Frankel W., Costa R., et al. Metallothionein expression is suppressed in primary human hepatocellular carcinomas and is mediated through inactivation of CCAAT/enhancer binding protein alpha by phosphatidylinositol 3-kinase signaling cascade. Cancer Res 2007, 67:2736-2746.
60. Haase H., Maret W. Protein tyrosine phosphatases as targets of the combined insulinomimetic effects of zinc and oxidants. Biometals 2005, 18:333-338.
61. Jansen J., Karges W., Rink L. Zinc and diabetes - clinical links and molecular mechanisms. J Nutr Biochem 2009, 20:399-417.
62. Basuki W., Hiromura M., Sakurai H. Insulinomimetic Zn complex (Zn(opt)2) enhances insulin signaling pathway in 3T3-L1 adipocytes. J Inorg Biochem 2007, 101:692-699.