Role of AMP-activated protein kinase in ferritin H gene expression by resveratrol in human T cells

Biochemistry

Volumn 52, Issue 30, 2013, Pages 5075-5083

  Iwasaki, Kenta ^a   Ray, Paul D ^b   Huang, Bo Wen ^b   Sakamoto, Kensuke ^b   Kobayashi, Takaaki ^a   Tsuji, Yoshiaki ^b  

^a NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMP-ACTIVATED PROTEIN KINASE; ANTIOXIDANT CAPACITY; ANTIOXIDANT RESPONSIVE ELEMENTS; CHROMATIN IMMUNOPRECIPITATION ASSAY; GLYCOGEN SYNTHASE KINASE-3; HUMAN PERIPHERAL BLOOD; NUCLEAR ACCUMULATION; TRANSCRIPTIONAL ACTIVATIONS;

CELL SIGNALING; CHEMICAL COMPOUNDS; GENES; PHOSPHORYLATION; TRANSCRIPTION;

RESVERATROL;

CD3 ANTIGEN; FERRITIN; FERRITIN H; GLYCOGEN SYNTHASE KINASE 3BETA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; RESVERATROL; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; T LYMPHOCYTE; TRANSCRIPTION INITIATION;

AMP-ACTIVATED PROTEIN KINASES; ANTIOXIDANTS; APOFERRITINS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; JURKAT CELLS; K562 CELLS; LEUKOCYTES, MONONUCLEAR; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RESPONSE ELEMENTS; RNA INTERFERENCE; SERINE; STILBENES; T-LYMPHOCYTES;

EID: 84881071384     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400399f     Document Type: Article

References (46)

1. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T. D., Mazur, M., and Telser, J. (2007) Free radicals and antioxidants in normal physiological functions and human disease Int. J. Biochem. Cell Biol. 9, 44-84
2. Kaminski, M. M., Sauer, S. W., and Klemke, C.-D. 2010, Mitochondrial reactive oxygen species control T cell activation by regulating IL-2 and IL-4 expression: Mechanism of ciprofloxacin-mediated immunosuppression J. Immunol. 184, 4827-4841
3. Larbi, A., Kempf, J., and Pawelec, G. (2007) Oxidative stress modulation and T cell activation Exp. Gerontol. 42, 852-858
4. Williams, M. S. and Kwon, J. (2004) T cell receptor stimulation, reactive oxygen species, and cell signaling Free Radical Biol. Med. 37, 1144-1151
5. Hildeman, D. A., Mitchell, T., and Teague, T. K. 1999, Reactive oxygen species regulate activation-induced T cell apoptosis Immunity 10, 735-744
6. Reichard, J. F., Motz, G. T., and Puga, A. (2007) Heme oxygenase-1 induction by NRF2 requires inactivation of the transcriptional repressor BACH1 Nucleic Acids Res. 35, 7074-7086
7. Zhang, J. Y., Ohta, T., and Maruyama, A. 2006, BRG1 interacts with Nrf2 to selectively mediate HO-1 induction in response to oxidative stress Mol. Cell. Biol. 26, 7942-7952
8. Gehm, B. D., McAndrews, J. M., Chien, P. Y., and Jameson, J. L. (1997) Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor Proc. Natl. Acad. Sci. U.S.A. 94, 14138-14143
9. Jang, M. S., Cai, E. N., and Udeani, G. O. 1997, Cancer chemopreventive activity of resveratrol, a natural product derived from grapes Science 275, 218-220
10. Baur, J. A. and Sinclair, D. A. (2006) Therapeutic potential of resveratrol: The in vivo evidence Nat. Rev. Drug Discovery 5, 493-506
11. Chan, A. Y. M., Dolinsky, V. W., and Soltys, C. L. M. 2008, Resveratrol inhibits cardiac hypertrophy via AMP-activated protein kinase and Akt J. Biol. Chem. 283, 24194-24201
12. Tsuji, Y. (2005) JunD activates transcription of the human ferritin H gene through an antioxidant response element during oxidative stress Oncogene 24, 7567-7578
13. Iwasaki, K., MacKenzie, E. L., Hailemariam, K., Sakamoto, K., and Tsuji, Y. (2006) Hemin-mediated regulation of an antioxidant-responsive element of the human ferritin H gene and role of Ref-1 during erythroid differentiation of K562 cells Mol. Cell. Biol. 26, 2845-2856
14. Mackenzie, E. L., Iwasaki, K., and Tsuji, Y. (2008) Intracellular iron transport and storage: From molecular mechanisms to health implications Antioxid. Redox Signaling 10, 997-1030
15. Puig, S., Askeland, E., and Thiele, D. J. (2005) Coordinated remodeling of cellular metabolism during iron deficiency through targeted mRNA degradation Cell 120, 99-110
16. Ferreira, C., Bucchini, D., and Martin, M. E. 2000, Early embryonic lethality of H ferritin gene deletion in mice J. Biol. Chem. 275, 3021-3024
17. Sakamoto, K., Iwasaki, K., Sugiyama, H., and Tsuji, Y. (2009) Role of the Tumor Suppressor PTEN in Antioxidant Responsive Element-mediated Transcription and Associated Histone Modifications Mol. Biol. Cell 20, 1606-1617
18. Papaiahgari, S., Zhang, Q., Yleeberger, S. R., Cho, H. Y., and Reddy, S. P. (2006) Hyperoxia stimulates an Nrf2-ARE transcriptional response via ROS-EGFR-PI3K-Akt/ERK MAP kinase signaling in pulmonary epithelial cells Antioxid. Redox Signaling 8, 43-52
19. Venkatachalam, K., Mummidi, S., Cortez, D. M., Prabhu, S. D., Valente, A. J., and Chandrasekar, B. (2008) Resveratrol inhibits high glucose-induced PI3K/Akt/ERK-dependent interleukin-17 expression in primary mouse cardiac fibroblasts Am. J. Physiol. 294, H2078-H2087
20. Baur, J. A., Pearson, K. J., and Price, N. L. 2006, Resveratrol improves health and survival of mice on a high-calorie diet Nature 444, 337-342
21. Ruderman, N. and Prentki, M. (2004) AMP kinase and malonyl-CoA: Targets for therapy of the metabolic syndrome Nat. Rev. Drug Discovery 3, 340-351
22. Nath, N., Khan, M., Paintlia, M. K., Hoda, M. N., and Giri, S. (2009) Metformin Attenuated the Autoimmune Disease of the Central Nervous System in Animal Models of Multiple Sclerosis J. Immunol. 182, 8005-8014
23. Pervaiz, S. and Holme, A. L. (2009) Resveratrol: Its biologic targets and functional activity Antioxid. Redox Signaling 11, 2851-2897
24. Salazar, M., Rojo, A. I., Velasco, D., de Sagarra, R. M., and Cuadrado, A. (2006) Glycogen synthase kinase-3β inhibits the xenobiotic and antioxidant cell response by direct phosphorylation and nuclear exclusion of the transcription factor Nrf2 J. Biol. Chem. 281, 14841-14851
25. Rada, P., Rojo, A. I., Chowdhry, S., McMahon, M., Hayes, J. D., and Cuadrado, A. (2011) SCF/β-TrCP Promotes Glycogen Synthase Kinase 3-Dependent Degradation of the Nrf2 Transcription Factor in a Keap1-Independent Manner Mol. Cell. Biol. 31, 1121-1133
26. Ray, P. D., Huang, B.-W., and Tsuji, Y. (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling Cell. Signalling 24, 981-990
27. MacKenzie, E. L., Ray, P. D., and Tsuji, Y. (2008) Role and regulation of ferritin H in rotenone-mediated mitochondrial oxidative stress Free Radical Biol. Med. 44, 1762-1771
28. Canto, C. and Auwerx, J. (2010) AMP-activated protein kinase and its downstream transcriptional pathways Cell. Mol. Life Sci. 67, 3407-3423
29. Choi, S. H., Kim, Y. W., and Kim, S. G. (2010) AMPK-mediated GSK3β inhibition by isoliquiritigenin contributes to protecting mitochondria against iron-catalyzed oxidative stress Biochem. Pharmacol. 79, 1352-1362
30. Martin, D., Rojo, A. I., and Salinas, M. 2004, Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol J. Biol. Chem. 279, 8919-8929
31. Iwasaki, K., Miwa, Y., Haneda, M., Uchida, K., Nakao, A., and Kobayashi, T. (2010) Significance of HLA class I antibody-induced antioxidant gene expression for endothelial cell protection against complement attack Biochem. Biophys. Res. Commun. 391, 1210-1215
32. Frojdo, S., Cozzone, D., Vidal, H., and Pirola, L. (2007) Resveratrol is a class IA phosphoinositide 3-kinase inhibitor Biochem. J. 406, 511-518
33. He, X., Wang, Y., Zhu, J., Orloff, M., and Eng, C. (2011) Resveratrol enhances the anti-tumor activity of the mTOR inhibitor rapamycin in multiple breast cancer cell lines mainly by suppressing rapamycin-induced AKT signaling Cancer Lett. 301, 168-176
34. Shimokawa, I. and Trindade, L. S. (2010) Dietary restriction and aging in rodents: A current view on its molecular mechanisms Aging and Disease 1, 89-107
35. Onken, B. and Driscoll, M. (2010) Metformin Induces a Dietary Restriction-Like State and the Oxidative Stress Response to Extend C. elegans Healthspan via AMPK, LKB1, and SKN-1 PLoS One 5, e8758
36. Kim, Y. I., Cho, J. H., Yoo, O. J., and Ahnn, J. (2004) Transcriptional regulation and life-span modulation of cytosolic aconitase and ferritin genes in C. elegans J. Mol. Biol. 342, 421-33
37. Hedrick, S. M., Michelini, R. H., Doedens, A. L., Goldrath, A. W., and Stone, E. L. (2012) FOXO transcription factors throughout T cell biology Nat. Rev. Immunol. 12, 649-661
38. Devadas, S., Zaritskaya, L., Rhee, S. G., Oberley, L., and Williams, M. S. (2002) Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: Selective regulation of mitogen-activated protein kinase activation and Fas ligand expression J. Exp. Med. 195, 59-70
39. 2+ in T lymphocytes J. Exp. Med. 203, 1665-1670
40. Lee, J. Y., Choi, A. Y., and Oh, Y. T. 2012, AMP-activated protein kinase mediates T cell activation-induced expression of FasL and COX-2 via protein kinase Cθ-dependent pathway in human Jurkat T leukemia cells Cell. Signalling 24, 1195-1207
41. Zheng, Y., Delgoffe, G. M., Meyer, C. F., Chan, W., and Powell, J. D. (2009) Anergic T Cells Are Metabolically Anergic J. Immunol. 183, 6095-6101
42. Chauveau, C., Remy, S., and Royer, P. J. 2005, Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression Blood 106, 1694-1702
43. Schmielau, J. and Finn, O. J. (2001) Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients Cancer Res. 61, 4756-4760
44. Kaur, D., Yantiri, F., and Rajagopalan, S. 2003, Genetic or pharmacological iron chelation prevents MPTP-induced neurotoxicity in vivo: A novel therapy for Parkinson's disease Neuron 37, 899-909
45. Orino, K., Lehman, L., Tsuji, Y., Ayaki, H., Torti, S. V., and Torti, F. M. (2001) Ferritin and the response to oxidative stress Biochem. J. 357, 241-247
46. Pham, C. G., Bubici, C., and Zazzeroni, F. 2004, Ferritin heavy chain upregulation by NF-κB inhibits TNFα-induced apoptosis by suppressing reactive oxygen species Cell 119, 529-542