Black tea polyphenols mimic insulin/insulin-like growth factor-1 signalling to the longevity factor FOXO1a

Aging Cell

Volumn 7, Issue 1, 2008, Pages 69-77

  Cameron, Amy R ^a   Anton, Siobhan ^a,c   Melville, Laura ^a,d   Houston, Nicola P ^a,b,e   Dayal, Saurabh ^a   Mcdougall, Gordon J ^b   Stewart, Derek ^b   Rena, Graham ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c Gentian AS   (Norway)

^d MRC Reproductive Biology Unit   (United Kingdom)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Akt; Diabetes; FOXO1a; Insulin; PEPCK; Theaflavin

Indexed keywords

BLACK TEA EXTRACT; EPIGALLOCATECHIN GALLATE; INSULIN; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); POLYPHENOL DERIVATIVE; SOMATOMEDIN C; THEAFLAVIN 3,3' DIGALLATE; THEAFLAVINE 3' GALLATE; THEARUBIGIN; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG;

AGING; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG STRUCTURE; HUMAN; HUMAN CELL; LONGEVITY; METABOLIC DISORDER; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; BIFLAVONOIDS; CATECHIN; CELL LINE; FLAVONOIDS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; LONGEVITY; PHENOLS; PROTEIN-SERINE-THREONINE KINASES; RATS; SIGNAL TRANSDUCTION; TEA;

CAMELLIA SINENSIS; INVERTEBRATA; MAMMALIA; VERTEBRATA;

EID: 38349167559     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2007.00353.x     Document Type: Article

References (54)

1. Anton S, Melville L, Rena G (2007) The green tea constituent epigallocatechin gallate (EGCG) induces FOXO1a phosphorylation and augments the cellular response to insulin. Cell Signal. 19, 377-383.
2. Baba T, Shimizu T, Suzuki Y-I, Ogawara M, Isono K-I, Koseki H, Kurosawa H, Shirasawa T (2005) Estrogen, insulin, and dietary signals cooperatively regulate longevity signals to enhance resistance to oxidative stress in mice. J. Biol. Chem. 280, 16417-16426.
3. Biggs WH, Meisenhelder J, Hunter T, Cavenee WK, Arden KC (1999) Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc. Natl. Acad. Sci. USA 96, 7421-7426.
4. Brownawell AM, Kops, MI, Burgering BMT (2001) Inhibition of nuclear import by protein kinase B (Akt) regulates the subcellular distribution and activity of the forkhead transcription factor AFX. Mol. Cell. Biol. 21, 3534-3546.
5. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 96, 857-868.
6. Brunet A, Park J, Tran H, Hu LS, Hemmings BA, Greenberg ME (2001) Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol. Cell. Biol. 21, 952-965.
7. Brunet A, Kanai F, Stehn J, Xu J, Sarbassova Frangioni JV, Dalal SN, DeCaprio JA, Greenberg ME, Yaffe MB (2002) 14-3-3 Transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J. Cell. Biol. 156, 817-828.
8. Cao H, Hininger-Favier I, Kelly MA, Benaraba R., Dawson HD, Coves S, Roussel AM, Anderson RA (2007) Green tea polyphenol extract regulates the expression of genes involved in glucose uptake and insulin signaling in rats fed a high fructose diet. J. Agric. Food Chem. 55, 6372-6378.
9. Chippindale AK, Leroi AM, Kim SB, Rose MR (1993) Phenotypic plasticity and selection in Drosophila life-history evolution. 1. Nutrition and the cost of reproduction. J. Evol. Biol. 6, 171-193.
10. del Peso L, Gonzalez VM, Hernandez R., Barr FG, Nunez G (1999) Regulation of the forkhead transcription factor FKHR, but not the PAX3-FKHR fusion protein, by the serine/threonine kinase Akt. Oncogene 18, 7328-7333.
11. Del Rio D, Stewart AJ, Mullen W, Burns J, Lean MEJ, Brighenti F, Crozier A (2004) HPLC-MSn analysis of phenolic compounds and purine alkaloids in green and black tea. J. Agric. Food Chem. 52, 2807-2815.
12. Dong X, Park S, Lin X, Copps K, Yi X, White MF (2006) Irs1 and Irs2 signaling is essential for glucose homeostastis and systemic growth. J. Clin. Invest. 116, 101-114.
13. Forest CD, O'Brien RM, Lucas PC, Magnuson MA, Granner DK (1990) Regulation of phosphoenolpyruvate carboxykinase gene expression by insulin. Use of the stable transfection approach to locate an insulin responsive sequence. Mol. Endocrinol. 4, 1302-1310.
14. Gardner EJ, Ruxton CHS, Leeds AR (2007) Black tea -helpful or harmful? A review of the evidence. Eur. J. Clin. Nutr. 61, 3-18.
15. Giannakou ME, Goss M, Jünger MA, Hafen E, Leevers SJ, Partridge L (2004) Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science 305, 361.
16. Guo SD, Rena G, Cichy S, He XW, Cohen P, Unterman T (1999) Phosphorylation of serine 256 by protein kinase B disrupts transactivation by FKHR and mediates effects of insulin on insulin- like growth factor-binding protein-1 promoter activity through a conserved insulin response sequence. J. Biol. Chem. 274, 17184-17192.
17. Halliwell B, Rafter J, Jenner A (2005) Health promotion by flavonoids, tocopherols, tocotrienols and other phenols: Direct or indirect effects? Antioxidant or not? Am. J. Clin. Nutr. 81, 268S-276S.
18. van der Heide LP, Hoekman MFM, Smidt MP (2004) The ins and outs of FOXO shuttling: Mechanisms of FOXO translocation and transcriptional regulation. Biochem. J. 380, 297-309.
19. Hou Z, Sang S, You H, Lee MJ, Hong J, Chin K-V, Yang CS (2005) Mechanism of action of (-)-epigallocatechin-3-gallate: Auto-oxidation-dependent inactivation of epidermal growth factor receptor and direct effects on growth inhibition in human esophageal cancer KYSE 150 cells. Cancer Res. 65, 8049.
20. Jacobs FMJ, van der Heide LP, Wijchers PJEC, Burbach JPH, Hoekman MFM, Smidt MP (2003) FOXO6, a novel member of the FOXO class of transcription factors with distinct shuttling dynamics. J. Biol. Chem. 278, 35959-35967.
21. Kao YH, Hiipakka RA, Liao SS (2000) Modulation of endocrine systems and food intake by green tea epigallocatechin gallate. Endocrinology 141, 980-987.
22. Klass MR (1977) Aging in the nematode Caenorhabditis elegans: Major biological and environmental factors influencing life span. Mech. Ageing Dev. 6, 413-429.
23. Kops GJPL, de Ruiter ND, De Vriets-Smits AMM, Powell DR, Bos JL, Burgering BMT (1999) Direct control of the forkhead transcription factor AFX by protein kinase B. Nature 398, 630-634.
24. Kyle JAM, Morrice PC, McNeill G, Duthie GG (2007) Effects of infusion time and addition of milk on content and absorption of polyphenols from black tea. J. Agric. Food Chem. 55, 4889-4894.
25. Lin K, Dorman JB, Rodan A, Kenyon C (1997) daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278, 1319-1322.
26. Lochhead P, Rice SQJ, Sutherland C (2001) Inhibition of GSK-3 selectively reduces glucose 6-phosphatase and phosphoenolpyruvate carboxykinase gene expression. Diabetes 50, 937-946.
27. Logie L, Ruiz-Alcaraz AJ, Keane M, Woods YL, Bain J, Marquez R., Alessi DR, Sutherland C (2007) Characterisation of a protein kinase B inhibitor in vitro and in insulin treated liver cells. Diabetes 56, 2218-2227.
28. Lotito SB, Frei B (2006) Consumption of flavonoid-rich foods and increased plasma antioxidant capacity in humans: Cause, consequence, or epiphenomenon? Free Radic. Biol. Med. 41, 1727-1746.
29. Mair W, Piper MDW, Partridge L (2005) Calories do not explain extension of life span by dietary restriction in Drosophila. PLoS Biology 3, e223.
30. McCay CM, Crowell MF, Maynard LA (1935) The effect of retarded growth upon the length of life span and upon the ultimate body size. J. Nutr. 10, 63-79.
31. Nakae J, Park BC, Accili D (1999) Insulin stimulates phosphorylation of the forkhead transcription factor FKHR on serine 253 through wortmannin-sensitive pathway. J. Biol. Chem. 274, 15982-15985.
32. Nakae J, Barr V, Accili D (2000) Differential regulation of gene expression by insulin and IGF-1 receptors correlates with phosphorylation of a single amino acid residue in the forkhead transcription factor FKHR. EMBO J. 19, 989-996.
33. Nakae J, Biggs WH III, Kitamura T, Cavenee WK, Wright CVE, Arden KC, Accili D (2002) Regulation of insulin action and pancreatic-cell function by mutated alleles of the gene encoding forkhead transcription factor FOXO1. Nature Genet. 32, 245-253.
34. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G (1997) The fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C-elegans. Nature 389, 994-999.
35. Patel S, Lochhead PA, Rena G, Fumagalli S, Pende M, Kozma SC, Thomas G, Sutherland C (2002) Insulin regulation of insulin-like growth factor-binding protein-1 gene expression is dependent on the mammalian target of rapamycin, but independent of ribosomal S6 kinase activity. J. Biol. Chem. 277, 9889-9895.
36. Patel S, Lipina C, Sutherland C (2003) Different mechanisms are used by insulin to repress three genes that contain homologous thymine-rich insulin response elements. FEBS Lett. 549, 72-76.
37. Potenza MA, Marasciulo FL, Tarquinio M, Tiravanti E, Colantuono G, Federici A, Kim J-A, Quon MJ, Montagnani M (2007) EGCG, a green tea polyphenol, improves endothelial function and insulin sensitivity, reduces blood pressure and protects against myocardial I/R injury in SHR. Am. J. Physiol. Endocrinol. Metab. 292, E1378-E1387.
38. Rena G, Guo SD, Cichy SC, Unterman TG, Cohen P (1999) Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J. Biol. Chem. 274, 17179-17183.
39. Rena G, Prescott AR, Guo SD, Cohen P, Unterman TG (2001) Roles of the forkhead in rhabdomyosarcoma (FKHR) phosphorylation sites in regulating 14-3-3 binding, transactivation and nuclear targetting. Biochem. J. 354, 605-612.
40. Rena G, Woods YL, Prescott AR, Peggie M, Unterman TG, Williams MR, Cohen P (2002) Two novel phosphorylation sites on FKHR that are critical for its nuclear exclusion. EMBO J. 21, 2263-2271.
41. Rena G, Bain J, Elliott M, Cohen P (2004) D4476 a cell-permeant inhibitor of CK1 suppresses the site-specific phosphorylation and nuclear exclusion of FOXO1a. EMBO Reports 5, 60-65.
42. Samuel VT, Choi CS, Phillips TG, Romanelli AJ, Geisler JG, Bhanot S, McKay RM, Monia B, Shutter JR, Lindberg RA, Shulman GI, Veniant MM (2006) Targeting FOXO1 in mice using antisense oligonucleotide improves hepatic and peripheral insulin action. Diabetes 55, 2042-2050.
43. Shulman GI (2000) Cellular mechanisms of insulin resistance. J. Clin. Invest. 106, 171-176.
44. Takaishi H, Konishi H, Matsuzaki H, Ono Y, Shirai Y, Saito N, Kitamura T, Ogawa W, Kasuga M, Kikkawa U, Nishizuka Y (1999) Regulation of nuclear translocation of Forkhead transcription factor AFX by protein kinase B. Proc. Natl. Acad. Sci. USA 96, 11836-11841.
45. Tang ED, Nunez G, Barr FG, Guan KL (1999) Negative regulation of the forkhead transcription factor FKHR by Akt. J. Biol. Chem. 274, 16741-16746.
46. Waltner-Law ME, Wang XL, Law BK, Hall RK, Nawano M, Granner DK (2002) Epigallocatechin gallate, a constituent of green tea, represses hepatic glucose production. J. Biol. Chem. 277, 34933-34940.
47. Weindruch R, Walford RL (1982) Dietary restriction in mice beginning at 1 year of age: Effect on life-span and spontaneous cancer incidence. Science 215, 1415-1418.
48. Wiseman S, Mulder T, Rietveld A (2001) Tea flavonoids: Bioavailability in vivo and effects on cell signaling pathways in vitro. Antioxid. Redox Signal. 3, 1009-1021.
49. Wolfram S, Raederstorff D, Preller M, Wang Y, Teixeira SR, Riegger C, Weber P (2006) Epigallocatechin gallate supplementation alleviates diabetes in rodents. J. Nutr. 136, 2512-2518.
50. Woods YL, Rena G, Morrice N, Barthel A, Becker W, Guo S, Unterman TG, Cohen P (2001) The kinase DYRK1A phosphorylates the transcription factor FKHR at Ser329 in vitro, a novel in vivo phosphorylation site. Biochem. J. 355, 597-607.
51. Yuan M, Konstantopoulos N, Lee J, Hansen L, Li Z-W, Karin M, Shoelson S (2001) Reversal of obesity and diet-induced insulin resistance with salicylates or targeted disruption of Ikk beta. Science 293, 1673-1677.
52. Zhang W, Patil S, Chauhan B, Guo S, Powell DR, Le Angelos Klotsas J, Matika R., Xiao X, Heidenrich KA, Sajan MP, Farese RV, StolZ. DB, Tso P, Koo S-H, Montminy M, Unterman TG (2006) FOXO1 regulates multiple metabolic pathways in the liver. J. Biol. Chem. 281, 10105-10117.
53. Zhao XS, Gan LX, Pan HY, Kan DH, Majeski M, Adam SA, Unterman TG (2004) Multiple elements regulate nuclear/cytoplasmic shuttling of FOX01: characterization of phosphorylation- and 14-3-3-dependent and -independent mechanisms. Biochem. J. 378, 839-849.
54. Zimmet P, Alberti KGMM, Shaw J (2001) Global and societal implications of the diabetes epidemic. Nature 414, 782-787.