Resveratrol increases anti-aging Klotho gene expression via the activating transcription factor 3/c-Jun complex-mediated signaling pathway

International Journal of Biochemistry and Cell Biology

Volumn 53, Issue , 2014, Pages 361-371

  Hsu, Shih Che ^a   Huang, Shih Ming ^a   Chen, Ann ^a,b   Sun, Chiao Yin ^c,d   Lin, Shih Hua ^a,b   Chen, Jin Shuen ^a,b   Liu, Shu Ting ^a   Hsu, Yu Juei ^a,b  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^d CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

Activating transcription factor 3 (ATF3); Anti aging; c Jun; Klotho; Resveratrol

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; KLOTHO PROTEIN; PROTEIN C JUN; RESVERATROL; SIRTUIN 1; ATF3 PROTEIN, MOUSE; BETA GLUCURONIDASE; MESSENGER RNA; STILBENE DERIVATIVE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; CHROMATIN IMMUNOPRECIPITATION; EPITHELIUM CELL; GENE EXPRESSION; GENE FUNCTION; HUMAN; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CELL; KIDNEY PARENCHYMA; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSIENT TRANSFECTION; UPREGULATION; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; GENE EXPRESSION REGULATION; GLUCURONIDASE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIRTUIN 1; STILBENES; TRANSCRIPTION FACTOR AP-1;

EID: 84903123965     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2014.06.002     Document Type: Article

References (53)

1. K. Ameri, E.M. Hammond, C. Culmsee, M. Raida, D.M. Katschinski, R.H. Wenger, E. Wagner, R.J. Davis, T. Hai, N. Denko, and A.L. Harris Induction of activating transcription factor 3 by anoxia is independent of p53 and the hypoxic HIF signalling pathway Oncogene 26 2007 284 289 (Pubitemid 46095739)
2. J.A. Baur, and D.A. Sinclair Therapeutic potential of resveratrol: the in vivo evidence Nat Rev Drug Discovery 5 2006 493 506 (Pubitemid 44136961)
3. A. Brunet, L.B. Sweeney, J.F. Sturgill, K.F. Chua, P.L. Greer, Y. Lin, H. Tran, S.E. Ross, R. Mostoslavsky, H.Y. Cohen, L.S. Hu, H.L. Cheng, M.P. Jedrychowski, S.P. Gygi, D.A. Sinclair, F.W. Alt, and M.E. Greenberg Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase Science 303 2004 2011 2015 (Pubitemid 38393275)
4. B.P. Chen, C.D. Wolfgang, and T. Hai Analysis of ATF3, a transcription factor induced by physiological stresses and modulated by gadd153/Chop10 Mol Cell Biol 16 1996 1157 1168 (Pubitemid 26061687)
5. K.N. Cho, M. Sukhthankar, S.H. Lee, J.H. Yoon, and S.J. Baek Green tea catechin (-)-epicatechin gallate induces tumour suppressor protein ATF3 via EGR-1 activation Eur J Cancer 43 2007 2404 2412 (Pubitemid 47625970)
6. B.H. Choi, C.G. Kim, Y. Lim, Y.H. Lee, and S.Y. Shin Transcriptional activation of the human Klotho gene by epidermal growth factor in HEK293 cells; role of Egr-1 Gene 450 2010 121 127
7. S. Chung, H. Yao, S. Caito, J.W. Hwang, G. Arunachalam, and I. Rahman Regulation of SIRT1 in cellular functions: role of polyphenols Arch Biochem Biophys 501 2010 79 90
8. A. Csiszar, N. Labinskyy, R. Jimenez, J.T. Pinto, P. Ballabh, G. Losonczy, K.J. Pearson, R. de Cabo, and Z. Ungvari Anti-oxidative and anti-inflammatory vasoprotective effects of caloric restriction in aging: role of circulating factors and SIRT1 Mech Ageing Dev 130 2009 518 527
9. C.A. de la Lastra, and I. Villegas Resveratrol as an anti-inflammatory and anti-aging agent: mechanisms and clinical implications Mol Nutr Food Res 49 2005 405 430 (Pubitemid 40780389)
10. I.J. Deary, S.E. Harris, H.C. Fox, C. Hayward, A.F. Wright, J.M. Starr, and L.J. Whalley KLOTHO genotype and cognitive ability in childhood and old age in the same individuals Neurosci Lett 378 2005 22 27 (Pubitemid 40341936)
11. S. Fulda, and K.M. Debatin Resveratrol modulation of signal transduction in apoptosis and cell survival: a mini-review Cancer Detect Prev 30 2006 217 223 (Pubitemid 44163050)
12. T. Hai, and M.G. Hartman The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: activating transcription factor proteins and homeostasis Gene 273 2001 1 11 (Pubitemid 32718721)
13. T. Hai, C.D. Wolfgang, D.K. Marsee, A.E. Allen, and U. Sivaprasad ATF3 and stress responses Gene Expression 7 1999 321 335 (Pubitemid 29372076)
14. K.B. Harikumar, and B.B. Aggarwal Resveratrol: a multitargeted agent for age-associated chronic diseases Cell Cycle 7 2008 1020 1035
15. J.R. Jackson, M.J. Ryan, and S.E. Alway Long-term supplementation with resveratrol alleviates oxidative stress but does not attenuate sarcopenia in aged mice J Gerontol, Ser A: Biol Sci Med Sci 66 2011 751 764
16. J.R. Jackson, M.J. Ryan, Y. Hao, and S.E. Alway Mediation of endogenous antioxidant enzymes and apoptotic signaling by resveratrol following muscle disuse in the gastrocnemius muscles of young and old rats Am J Physiol Regul Integr Comp Physiol 299 2010 R1572 R1581
17. K. Kawano, and H. Kawaguchi Human klotho gene polymorphisms associated with bone density of aged postmenopausal women Nihon Rinsho 2 62 Suppl 2004 190 194
18. D.H. Kim, Y.J. Jung, J.E. Lee, A.S. Lee, K.P. Kang, S. Lee, S.K. Park, M.K. Han, S.Y. Lee, K.M. Ramkumar, M.J. Sung, and W. Kim SIRT1 activation by resveratrol ameliorates cisplatin-induced renal injury through deacetylation of p53 Am J Physiol Renal Physiol 301 2011 F427 F435
19. S. Kiryu-Seo, R. Kato, T. Ogawa, S. Nakagomi, K. Nagata, and H. Kiyama Neuronal injury-inducible gene is synergistically regulated by ATF3, c-Jun, and STAT3 through the interaction with Sp1 in damaged neurons J Biol Chem 283 2008 6988 6996
20. P. Kovacic, and R. Somanathan Multifaceted approach to resveratrol bioactivity: focus on antioxidant action, cell signaling and safety Oxid Med Cell Longevity 3 2010 86 100
21. M. Kuro-o Klotho in health and disease Curr Opin Nephrol Hypertens 21 2012 362 368
22. M. Kuro-o, Y. Matsumura, H. Aizawa, H. Kawaguchi, T. Suga, T. Utsugi, Y. Ohyama, M. Kurabayashi, T. Kaname, E. Kume, H. Iwasaki, A. Iida, T. Shiraki-Iida, S. Nishikawa, R. Nagai, and Y.I. Nabeshima Mutation of the mouse klotho gene leads to a syndrome resembling ageing Nature 390 1997 45 51 (Pubitemid 27494749)
23. S.H. Lee, J.H. Bahn, N.C. Whitlock, and S.J. Baek Activating transcription factor 2 (ATF2) controls tolfenamic acid-induced ATF3 expression via MAP kinase pathways Oncogene 29 2010 5182 5192
24. S.H. Lee, K. Yamaguchi, J.S. Kim, T.E. Eling, S. Safe, Y. Park, and S.J. Baek Conjugated linoleic acid stimulates an anti-tumorigenic protein NAG-1 in an isomer specific manner Carcinogenesis 27 2006 972 981
25. H.F. Li, C.F. Cheng, W.J. Liao, H. Lin, and R.B. Yang ATF3-mediated epigenetic regulation protects against acute kidney injury J Am Soc Nephrol 21 2010 1003 1013
26. G. Liang, C.D. Wolfgang, B.P. Chen, T.H. Chen, and T. Hai ATF3 gene. Genomic organization, promoter, and regulation J Biol Chem 271 1996 1695 1701
27. J.A. Moreno, M.C. Izquierdo, M.D. Sanchez-Nino, B. Suarez-Alvarez, C. Lopez-Larrea, A. Jakubowski, J. Blanco, R. Ramirez, R. Selgas, M. Ruiz-Ortega, J. Egido, A. Ortiz, and A.B. Sanz The inflammatory cytokines TWEAK and TNFalpha reduce renal klotho expression through NFkappaB J Am Soc Nephrol 22 2011 1315 1325
28. S. Nakagomi, Y. Suzuki, K. Namikawa, S. Kiryu-Seo, and H. Kiyama Expression of the activating transcription factor 3 prevents c-Jun N-terminal kinase-induced neuronal death by promoting heat shock protein 27 expression and Akt activation J Neurosci 23 2003 5187 5196 (Pubitemid 36793247)
29. T. Nakatani, M. Ohnishi, and M.S. Razzaque Inactivation of klotho function induces hyperphosphatemia even in presence of high serum fibroblast growth factor 23 levels in a genetically engineered hypophosphatemic (Hyp) mouse model FASEB J 23 2009 3702 3711
30. S. Nonomura, H. Kanagawa, and A. Makimoto Chemical constituents of polygonaceous plants I. Studies on the components of Ko-J O-Kon. (Polygonum Cuspidatum Sieb. Et Zucc.)] Yakugaku Zasshi 83 1963 988 990
31. P.S. Pardo, and A.M. Boriek An autoregulatory loop reverts the mechanosensitive Sirt1 induction by EGR1 in skeletal muscle cells Aging (Albany, NY) 4 2012 456 461
32. S.J. Park, F. Ahmad, A. Philp, K. Baar, T. Williams, H. Luo, H. Ke, H. Rehmann, R. Taussig, A.L. Brown, M.K. Kim, M.A. Beaven, A.B. Burgin, V. Manganiello, and J.H. Chung Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases Cell 148 2012 421 433
33. I. Pavik, P. Jaeger, L. Ebner, C.A. Wagner, K. Petzold, D. Spichtig, D. Poster, R.P. Wuthrich, S. Russmann, and A.L. Serra Secreted Klotho and FGF23 in chronic kidney disease Stage 1 to 5: a sequence suggested from a cross-sectional study Nephrol Dial Transplant 28 2013 352 359
34. J.H. Ren, Y. Tao, Z.Z. Zhang, W.X. Chen, X.F. Cai, K. Chen, B.C. Ko, C.L. Song, L.K. Ran, W.Y. Li, A.L. Huang, and J. Chen Sirtuin 1 regulates hepatitis B virus transcription and replication by targeting transcription factor AP-1 J Virol 88 2014 2442 2451
35. E.J. Rhee, K.W. Oh, W.Y. Lee, S.Y. Kim, C.H. Jung, B.J. Kim, K.C. Sung, B.S. Kim, J.H. Kang, M.H. Lee, S.W. Kim, and J.R. Park The differential effects of age on the association of KLOTHO gene polymorphisms with coronary artery disease Metabolism 55 2006 1344 1351
36. M. Satoh, H. Nagasu, Y. Morita, T.P. Yamaguchi, Y.S. Kanwar, and N. Kashihara Klotho protects against mouse renal fibrosis by inhibiting Wnt signaling Am J Physiol Renal Physiol 303 2012 F1641 F1651
37. Y. Shimoyama, K. Nishio, N. Hamajima, and T. Niwa KLOTHO gene polymorphisms G-395A and C1818T are associated with lipid and glucose metabolism, bone mineral density and systolic blood pressure in Japanese healthy subjects Clin Chim Acta 406 2009 134 138
38. J.M. Smoliga, J.A. Baur, and H.A. Hausenblas Resveratrol and health - a comprehensive review of human clinical trials Mol Nutr Food Res 55 2011 1129 1141
39. H. Sugiura, T. Yoshida, M. Mitobe, S. Yoshida, S. Shiohira, K. Nitta, and K. Tsuchiya Klotho reduces apoptosis in experimental ischaemic acute kidney injury via HSP-70 Nephrol Dial Transplant 25 2010 60 68
40. R. Taub Liver regeneration 4: transcriptional control of liver regeneration FASEB J 10 1996 413 427
41. M.R. Thompson, D. Xu, and B.R. Williams ATF3 transcription factor and its emerging roles in immunity and cancer J Mol Med (Berl) 87 2009 1053 1060
42. P.U. Torres, D. Prie, V. Molina-Bletry, L. Beck, C. Silve, and G. Friedlander Klotho: an antiaging protein involved in mineral and vitamin D metabolism Kidney Int 71 2007 730 737 (Pubitemid 46624027)
43. K. Turan, and P. Ata Effects of intra- and extracellular factors on anti-aging klotho gene expression Genet Mol Res 10 2011 2009 2023
44. I. Urakawa, Y. Yamazaki, T. Shimada, K. Iijima, H. Hasegawa, K. Okawa, T. Fujita, S. Fukumoto, and T. Yamashita Klotho converts canonical FGF receptor into a specific receptor for FGF23 Nature 444 2006 770 774 (Pubitemid 44949607)
45. T. Utsugi, T. Ohno, Y. Ohyama, T. Uchiyama, Y. Saito, Y. Matsumura, H. Aizawa, H. Itoh, M. Kurabayashi, S. Kawazu, S. Tomono, Y. Oka, T. Suga, M. Kuro-o, Y. Nabeshima, and R. Nagai Decreased insulin production and increased insulin sensitivity in the klotho mutant mouse, a novel animal model for human aging Metabolism 49 2000 1118 1123
46. H. van Dam, and M. Castellazzi Distinct roles of Jun: Fos and Jun: ATF dimers in oncogenesis Oncogene 20 2001 2453 2464 (Pubitemid 32531302)
47. W.M. Wang, S.T. Liu, S.M. Huang, W.S. Lin, S.G. Chen, and Y.L. Chang Zac1 functional interactions mediate AP-1 transcriptional activity Biochim Biophys Acta 1813 2011 2050 2060
48. Y. Wang, and Z. Sun Current understanding of klotho Ageing Res Rev 8 2009 43 51
49. N.C. Whitlock, J.H. Bahn, S.H. Lee, T.E. Eling, and S.J. Baek Resveratrol-induced apoptosis is mediated by early growth response-1 Kruppel-like factor 4, and activating transcription factor 3 Cancer Prev Res (Phila) 4 2011 116 127
50. K. Yamaguchi, S.H. Lee, J.S. Kim, J. Wimalasena, S. Kitajima, and S.J. Baek Activating transcription factor 3 and early growth response 1 are the novel targets of LY294002 in a phosphatidylinositol 3-kinase-independent pathway Cancer Res 66 2006 2376 2384
51. X. Yin, C.C. Wolford, Y.S. Chang, S.J. McConoughey, S.A. Ramsey, A. Aderem, and T. Hai ATF3, an adaptive-response gene, enhances TGF{beta} signaling and cancer-initiating cell features in breast cancer cells J Cell Sci 123 2010 3558 3565
52. H. Zhang, Y. Li, Y. Fan, J. Wu, B. Zhao, Y. Guan, S. Chien, and N. Wang Klotho is a target gene of PPAR-gamma Kidney Int 74 2008 732 739
53. R. Zhang, H.Z. Chen, J.J. Liu, Y.Y. Jia, Z.Q. Zhang, R.F. Yang, Y. Zhang, J. Xu, Y.S. Wei, D.P. Liu, and C.C. Liang SIRT1 suppresses activator protein-1 transcriptional activity and cyclooxygenase-2 expression in macrophages J Biol Chem 285 2010 7097 7110