Ligand-activated PPARδ inhibits UVB-induced senescence of human keratinocytes via PTEN-mediated inhibition of superoxide production

Biochemical Journal

Volumn 444, Issue 1, 2012, Pages 27-38

  Ham, SunAh ^a   Hwang, JungSeok ^a   Yoo, Taesik ^a   Lee, Hanna ^a   Kang, EunSil ^a   Park, Chankyu ^a   Oh, Jae Wook ^a   Lee, HoonTaek ^a   Min, Gyesik ^b   Kim, Jin Hoi ^a   Seo, Han Geuk ^a  

^a Konkuk University   (South Korea)

^b Gyeongsang National University   (South Korea)

Author keywords

Peroxisome proliferator activated receptor (PPAR ); Phosphatase and tensin homologue deleted on chromosome 10 (PTEN); Phosphatidylinositol 3 kinase (PI3K); Reactive oxygen species (ROS); Senescence; UVB

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; [2 METHYL 4 [4 METHYL 2 (4 TRIFLUOROMETHYLPHENYL) 5 THIAZOLYLMETHYLTHIO]PHENOXY]ACETIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; SUPEROXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CELL AGING; CELL COUNT; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME REPRESSION; GENE SILENCING; HAIRLESS MOUSE; HUMAN; HUMAN CELL; KERATINOCYTE; MELANOMA; MOUSE; NONHUMAN; PHOTOAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SKIN CANCER; ULTRAVIOLET B RADIATION; UPREGULATION;

ANIMALS; CELL AGING; CELL MEMBRANE; CELLS, CULTURED; CHILD; ENZYME ACTIVATION; HUMANS; KERATINOCYTES; LIGANDS; MICE; MICE, HAIRLESS; PHOSPHATIDYLINOSITOL 3-KINASES; PPAR DELTA; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RAC1 GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; SKIN; SUPEROXIDES; THIAZOLES; ULTRAVIOLET RAYS; UP-REGULATION;

MUS;

EID: 84860832705     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111832     Document Type: Article

References (49)

1. Hayflick, L. (1965) The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37, 614-636
2. Chen, Q. M., Prowse, K. R., Tu, V. C., Purdom, S. and Linskens, M. H. (2001) Uncoupling the senescent phenotype from telomere shortening in hydrogen peroxide-treated fibroblasts. Exp. Cell Res. 265, 294-303 (Pubitemid 32980218)
3. Harley, C. B., Futcher, A. B. and Greider, C. W. (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345, 458-460
4. Lewis, D. A., Yi, Q., Travers, J. B. and Spandau, D. F. (2008) UVB-induced senescence in human keratinocytes requires a functional insulin-like growth factor-1 receptor and p53. Mol. Biol. Cell 19, 1346-1353 (Pubitemid 351805090)
5. Holliday, R. (1986) Strong effects of 5-azacytidine on the in vitro lifespan of human diploid fibroblasts. Exp. Cell Res. 166, 543-552
6. Ogryzko, V. V., Hirai, T. H., Russanova, V. R., Barbie, D. A. and Howard, B. H. (1996) Human fibroblast commitment to a senescence-like state in response to histone deacetylase inhibitors is cell cycle dependent. Mol. Cell. Biol. 16, 5210-5218 (Pubitemid 26272174)
7. Mallette, F. A., Gaumont-Leclerc, M. F. and Ferbeyre, G. (2007) The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence. Genes Dev. 21, 43-48 (Pubitemid 46089705)
8. Assefa, Z., Laethem, A. V., Garmyn, M. and Agostinis, P. (2005) Ultaviolet radiation-induced apoptosis in keratinocytes: on the role of cytosolic factors. Biochim. Biophys. Acta. 1755, 90-106 (Pubitemid 40982560)
9. Madronich, S., McKenzie, R. L., Björn, L. O. and Caldwell, M. M. (1998) Changes in biologically active ultraviolet radiation reaching the Earth's surface. J. Photochem. Photobiol. B 46, 5-19 (Pubitemid 29017147)
10. von Zglinicki, T., Saretzki, G., Döcke, W. and Lotze, C. (1995) Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence? Exp. Cell Res. 220, 186-193
11. Hanson, K. M. and Clegg, R. M. (2002) Observation and quantification of ultraviolet-induced reactive oxygen species in ex vivo human skin. Photochem. Photobiol. 76, 57-63
12. Kang, S., Chung, J. H., Lee, J. H., Fisher, G. J., Wan, Y. S., Duell, E. A. and Voorhees, J. J. (2003) Topical N-acetyl cysteine and genistein prevent ultraviolet-light-induced signaling that leads to photoaging in human skin in vivo. J. Invest. Dermatol. 120, 835-841 (Pubitemid 36529087)
13. 2 is an important mediator of UVB-induced EGF-receptor phosphorylation in cultured keratinocytes. J. Invest. Dermatol. 110, 966-971
14. Valencia, A. and Kochevar, I. E. (2008) Nox1-based NADPH oxidase is the major source of UVA-induced reactive oxygen species in human keratinocytes. J. Invest. Dermatol. 128, 214-222 (Pubitemid 350249377)
15. Beak, S. M., Lee, Y. S. and Kim, J. A. (2004) NADPH oxidase and cyclooxygenase mediate the ultraviolet B-induced generation of reactive oxygen species and activation of nuclear factor-κB in HaCaT human keratinocytes. Biochimie 86, 425-429 (Pubitemid 39092705)
16. Ehrenborg, E. and Krook, A. (2009) Regulation of skeletal muscle physiology and metabolism by peroxisome proliferator-activated receptor δ. Pharmacol. Rev. 61, 373-393
17. Sertznig, P., Seifert, M., Tilgen, W. and Reichrath, J. (2008) Peroxisome proliferator-activated receptors (PPARs) and the human skin: importance of PPARs in skin physiology and dermatologic diseases. Am. J. Clin. Dermatol. 9, 15-31 (Pubitemid 351993189)
18. Bility, M. T., Zhu, B., Kang, B. H., Gonzalez, F. J. and Peters, J. M. (2010) Ligand activation of peroxisome proliferator-activated receptor-β/δ and inhibition of cyclooxygenase-2 enhances inhibition of skin tumorigenesis. Toxicol. Sci. 113, 27-36
19. Borland, M. G., Foreman, J. E., Girroir, E. E., Zolfaghari, R., Sharma, A. K., Amin, S., Gonzalez, F. J., Ross, A. C. and Peters, J. M. (2008) Ligand activation of peroxisome proliferator-activated receptor-β/δ inhibits cell proliferation in human HaCaT keratinocytes. Mol. Pharmacol. 74, 1429-1442
20. Tan, N. S., Michalik, L., Noy, N., Yasmin, R., Pacot, C., Heim, M., Flühmann, B., Desvergne, B. and Wahli, W. (2001) Critical roles of PPAR β/δ in keratinocyte response to inflammation. Genes Dev. 15, 3263-3277 (Pubitemid 34008192)
21. Tan, N. S., Michalik, L., Desvergne, B. and Wahli, W. (2005) Genetic- or transforming growth factor-β 1-induced changes in epidermal peroxisome proliferator-activated receptor β/δ expression dictate wound repair kinetics. J. Biol. Chem. 280, 18163-18170 (Pubitemid 41389061)
22. Ham, S. A., Kim, H. J., Kim, H. J., Kang, E. S., Eun, S. Y., Kim, G. H., Park, M. H., Woo, I. S., Kim, H. J., Chang, K. C. et al. (2010) PPARδ promotes wound healing by upregulating TGF-β1-dependent or -independent expression of extracellular matrix proteins. J. Cell. Mol. Med. 14, 1747-1759
23. Straface, E., Vona, R., Ascione, B., Matarrese, P., Strudthoff, T., Franconi, F. and Malorni, W. (2007) Single exposure of human fibroblasts (WI-38) to a sub-cytotoxic dose of UVB induces premature senescence. FEBS Lett. 581, 4342-4348 (Pubitemid 47301871)
24. Kim, H. J., Kang, S. Y., Kim, S. J., Kim, S. H. and Kim, T. Y. (2004) Potentiation of UVB-induced apoptosis by novel phytosphingosine derivative, tetraacetyl phytosphingosine in HaCaT cell and mouse skin. Apoptosis 9, 449-456 (Pubitemid 38987581)
25. Griendling, K. K., Minieri, C. A., Ollerenshaw, J. D. and Alexander, R. W. (1994) Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ. Res. 74, 1141-1148 (Pubitemid 24176909)
26. Fisher, G. J., Wang, Z. Q., Datta, S. C., Varani, J., Kang, S. and Voorhees, J. J. (1997) Pathophysiology of premature skin aging induced by ultraviolet light. N. Engl. J. Med. 337, 1419-1428 (Pubitemid 27497889)
27. Campisi, J. (2001) Cellular senescence as a tumor-suppressor mechanism. Trends Cell Biol. 11, S27-S31
28. Zhang, Q. S., Maddock, D. A., Chen, J. P., Heo, S., Chiu, C., Lai, D., Souza, K., Mehta, S. and Wan, Y. S. (2001) Cytokine-induced p38 activation feedback regulates the prolonged activation of AKT cell survival pathway initiated by reactive oxygen species in response to UV irradiation in human keratinocytes. Int. J. Oncol. 19, 1057-1061
29. Han, J. K., Lee, H. S., Yang, H. M., Hur, J., Jun, S. I., Kim, J. Y., Cho, C. H., Koh, G. Y., Peters, J. M., Park, K. W. et al. (2008) Peroxisome proliferator-activated receptor-δagonist enhances vasculogenesis by regulating endothelial progenitor cells through genomic and nongenomic activations of the phosphatidylinositol 3-kinase/Akt pathway. Circulation 118, 1021-1033
30. Stambolic, V., Suzuki, A., de la Pompa, J. L., Brothers, G. M., Mirtsos, C., Sasaki, T., Ruland, J., Penninger, J. M., Siderovski, D. P. and Mak, T. W. (1998) Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 95, 29-39 (Pubitemid 28458022)
31. Chiu, C., Maddock, D. A., Zhang, Q., Souza, K. P., Townsend, A. R. and Wan, Y. (2001) TGF-β-induced p38 activation is mediated by Rac1-regulated generation of reactive oxygen species in cultured human keratinocytes. Int. J. Mol. Med. 8, 251-255
32. Melnikova, V. O. and Ananthaswamy, H. N. (2005) Cellular and molecular events leading to the development of skin cancer. Mutat. Res. 571, 91-106 (Pubitemid 40313435)
33. Mullenders, L. H., van Hoffen, A., Vreeswijk, M. P., Ruven, H. J., Vrieling, H. and van Zeeland, A. A. (1997) Ultraviolet-induced photolesions: repair and mutagenesis. Recent Results Cancer Res. 143, 89-99
34. Kim, S. H., Kaminker, P. and Campisi, J. (2002) Telomeres, aging, and cancer: in search of a happy ending. Oncogene 21, 503-511 (Pubitemid 34146250)
35. Blackburn, E. H. (2005) Telomeres and telomerase: their mechanisms of action and the effects of altering their functions. FEBS Lett. 579, 859-862
36. Imanishi, T., Kobayashi, K., Kuroi, A., Ikejima, H. and Akasaka, T. (2008) Pioglitazone inhibits angiotensin II-induced senescence of endothelial progenitor cell. Hypertens. Res. 31, 757-765 (Pubitemid 351772867)
37. Gan, Q., Huang, J., Zhou, R., Niu, J., Zhu, X., Wang, J., Zhang, Z. and Tong, T. (2008) PPARγ accelerates cellular senescence by inducing p16INK4α expression in human diploid fibroblasts. J. Cell Sci. 121, 2235-2245
38. Jee, H. J., Kim, H. J., Kim, A. J., Bae, Y. S., Bae, S. S. and Yun, J. (2009) UV light induces premature senescence in Akt1-null mouse embryonic fibroblasts by increasing intracellular levels of ROS. Biochem. Biophys. Res. Commun. 383, 358-362
39. Seshiah, P. N., Weber, D. S., Rocic, P., Valppu, L., Taniyama, Y. and Griendling, K. K. (2002) Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ. Res. 91, 406-413 (Pubitemid 35034208)
40. Chow, L. M. and Baker, S. J. (2006) PTEN function in normal and neoplastic growth. Cancer Lett. 241, 184-196 (Pubitemid 44163047)
41. Stambolic, V., MacPherson, D., Sas, D., Lin, Y., Snow, B., Jang, Y., Benchimol, S. and Mak, T. W. (2001) Regulation of PTEN transcription by p53. Mol. Cell 8, 317-325 (Pubitemid 32831549)
42. Virolle, T., Adamson, E. D., Baron, V., Birle, D., Mercola, D., Mustelin, T. and de Belle, I. (2001) The Egr-1 transcription factor directly activates PTEN during irradiation-induced signalling. Nat. Cell Biol. 3, 1124-1128 (Pubitemid 33130464)
43. Burdick, A. D., Bility, M. T., Girroir, E. E., Billin, A. N., Willson, T. M., Gonzalez, F. J. and Peters, J. M. (2007) Ligand activation of peroxisome proliferator-activated receptor-β/δ(PPARβ/δ) inhibits cell growth of human N/TERT-1 keratinocytes. Cell. Signalling 19, 1163-1171 (Pubitemid 46561554)
44. Patel, L., Pass, I., Coxon, P., Downes, C. P., Smith, S. A. and Macphee, C. H. (2001) Tumor suppressor and anti-inflammatory actions of PPARγ agonists are mediated via upregulation of PTEN. Curr. Biol. 11, 764-768 (Pubitemid 32442793)
45. Zhang, W., Wu, N., Li, Z., Wang, L., Jin, J. and Zha, X. L. (2006) PPARγ activator rosiglitazone inhibits cell migration via upregulation of PTEN in human hepatocarcinoma cell line BEL-7404. Cancer Biol. Ther. 5, 1008-1014
46. Cantley, I. C. (2002) The phosphoinositide 3-kinase pathway. Science 296, 1655-1657
47. Ming, M., Han, W., Maddox, J., Soltani, K., Shea, C. R., Freeman, D. M. and He, Y. Y. (2010) UVB-induced ERK/AKT-dependent PTEN suppression promotes survival of epidermal keratinocytes. Oncogene 29, 492-502
48. Miyauchi, H., Minamino, T., Tateno, K., Kunieda, T., Toko, H. and Komuro, I. (2004) Akt negatively regulates the in vitro lifespan of human endothelial cells via a p53/p21-dependent pathway. EMBO J. 23, 212-220 (Pubitemid 38165761)
49. Kambayashi, H., Yamashita, M., Odake, Y., Takada, K., Funasaka, Y. and Ichihashi, M. (2001) Epidermal changes caused by chronic low-dose UV irradiation induce wrinkle formation in hairless mouse. J. Dermatol. Sci. 27, S19-S25