Naringenin protects HaCaT human keratinocytes against UVB-induced apoptosis and enhances the removal of cyclobutane pyrimidine dimers from the genome

Photochemistry and Photobiology

Volumn 84, Issue 2, 2008, Pages 307-316

  El Mahdy, Mohamed A ^a   Zhu, Qianzheng ^a   Wang, Qi En ^a   Wani, Gulzar ^a   Patnaik, Srinivas ^a   Zhao, Qun ^a   Arafa, El Shaimaa ^a   Barakat, Bassant ^a   Mir, Safita N ^a   Wani, Altaf A ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAVANONE DERIVATIVE; NARINGENIN; PYRIMIDINE DIMER;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CELL LINE; DRUG EFFECT; GENOME; HUMAN; ISOLATION AND PURIFICATION; KERATINOCYTE; MOLECULAR GENETICS; RADIATION EXPOSURE; ULTRAVIOLET RADIATION;

AMINO ACID SEQUENCE; APOPTOSIS; CELL LINE; FLAVANONES; GENOME, HUMAN; HUMANS; KERATINOCYTES; MOLECULAR SEQUENCE DATA; PYRIMIDINE DIMERS; ULTRAVIOLET RAYS;

CITRUS;

EID: 41049106041     PISSN: 00318655     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1751-1097.2007.00255.x     Document Type: Article

References (68)

1. Pourzand, C. R. M. Tyrrell (1999) Apoptosis, the role of oxidative stress and the example of solar UV radiation. Photochem. Photobiol. 70, 380 390.
2. Madronich, S., R. L. McKenzie, L. O. Bjorn M. M. Caldwell (1998) Changes in biologically active ultraviolet radiation reaching the Earth's surface. J. Photochem. Photobiol. B 46, 5 19.
3. Stewart, B. W., P. Kleihues, B. W. Stewart Y. Kletter (2003) World Cancer Report. IARC Press, Washington, DC.
4. Gailani, M. R., D. J. Leffell, A. Ziegler, E. G. Gross, D. E. Brash A. E. Bale (1996) Relationship between sunlight exposure and a key genetic alteration in basal cell carcinoma. J. Natl Cancer Inst. 88, 349 354.
5. Cleaver, J. E. E. Crowley (2002) UV damage, DNA repair and skin carcinogenesis. Front Biosci. 7, d1024 d1043.
6. Sarasin, A. (1999) The molecular pathways of ultraviolet-induced carcinogenesis. Mutat. Res. 428, 5 10.
7. de Gruijl, F. R. (2002) Photocarcinogenesis: UVA vs. UVB radiation. Skin Pharmacol. Appl. Skin Physiol. 15, 316 320.
8. Assefa, Z., L. A. Van, M. Garmyn P. Agostinis (2005) Ultraviolet radiation-induced apoptosis in keratinocytes: On the role of cytosolic factors. Biochim. Biophys. Acta 1755, 90 106.
9. Matsumura, Y. H. N. Ananthaswamy (2004) Toxic effects of ultraviolet radiation on the skin. Toxicol. Appl. Pharmacol. 195, 298 308.
10. Chen, Y. C., S. Y. Lin-Shiau J. K. Lin (1998) Involvement of reactive oxygen species and caspase 3 activation in arsenite-induced apoptosis. J. Cell. Physiol. 177, 324 333.
11. Chen, Y. C., S. C. Shen, W. R. Lee, F. L. Hsu, H. Y. Lin, C. H. Ko S. W. Tseng (2002) Emodin induces apoptosis in human promyeloleukemic HL-60 cells accompanied by activation of caspase 3 cascade but independent of reactive oxygen species production. Biochem. Pharmacol. 64, 1713 1724.
12. Bossy-Wetzel, E. D. R. Green (1999) Caspases induce cytochrome c release from mitochondria by activating cytosolic factors. J. Biol. Chem. 274, 17484 17490.
13. Nguyen, M., D. G. Millar, V. W. Yong, S. J. Korsmeyer G. C. Shore (1993) Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence. J. Biol. Chem. 268, 25265 25268.
14. Loeffler, M. G. Kroemer (2000) The mitochondrion in cell death control: Certainties and incognita. Exp. Cell Res. 256, 19 26.
15. De Laat, W. L., N. G. Jaspers J. H. Hoeijmakers (1999) Molecular mechanism of nucleotide excision repair. Genes Dev. 13, 768 785.
16. Lehmann, A. R. (1995) Nucleotide excision repair and the link with transcription. Trends Biochem. Sci. 20, 402 405.
17. Lindahl, T. R. D. Wood (1999) Quality control by DNA repair. Science 286, 1897 1905.
18. Narayana, K. R., M. S. Reddy, M. R. Chaluvadi D. R. Krishna (2001) Bioflavonoids classification, pharmacological, biochemical effects and therapeutic potential. Indian J. Pharmacol. 33, 2 16.
19. Mori, A., C. Nishinoc, N. Enoki S. Tawata (1988) Cytotoxicity of plant flavonoids against Hela cells. Phytochemistry 27, 1017 1020.
20. Maalouf, S., M. El-Sabban, N. Darwiche H. Gali-Muhtasib (2002) Protective effect of vitamin E on ultraviolet B light-induced damage in keratinocytes. Mol. Carcinog. 34, 121 130.
21. Gupta, S. H. Mukhtar (2002) Chemoprevention of skin cancer: Current status and future prospects. Cancer Metastasis Rev. 21, 363 380.
22. Bode, A. M. Z. Dong (2000) Signal transduction pathways: Targets for chemoprevention of skin cancer. Lancet Oncol. 1, 181 188.
23. Afaq, F., V. M. Adhami, N. Ahmad H. Mukhtar (2002) Botanical antioxidants for chemoprevention of photocarcinogenesis. Front Biosci. 7, d784 d792.
24. Einspahr, J. G., S. P. Stratton, G. T. Bowden D. S. Alberts (2002) Chemoprevention of human skin cancer. Crit. Rev. Oncol. Hematol. 41, 269 285.
25. Valenzuela, A., R. Guerra L. A. Videla (1986) Antioxidant properties of the flavonoids silybin and (+)-cyanidanol-3: Comparison with butylated hydroxyanisole and butylated hydroxytoluene. Planta Med. 52, 438 440.
26. Katiyar, S. K., N. J. Korman, H. Mukhtar R. Agarwal (1997) Protective effects of silymarin against photocarcinogenesis in a mouse skin model. J. Natl Cancer Inst. 89, 556 566.
27. Yang, C. S., J. M. Landau, M. T. Huang H. L. Newmark (2001) Inhibition of carcinogenesis by dietary polyphenolic compounds. Annu. Rev. Nutr. 21, 381 406.
28. Afaq, F., M. Saleem, C. G. Krueger, J. D. Reed H. Mukhtar (2005) Anthocyanin- and hydrolyzable tannin-rich pomegranate fruit extract modulates MAPK and NF-kappaB pathways and inhibits skin tumorigenesis in CD-1 mice. Int. J. Cancer 113, 423 433.
29. Williams, R. J., J. P. Spencer C. Rice-Evans (2004) Flavonoids: Antioxidants or signalling molecules? Free Radic. Biol. Med. 36, 838 849.
30. Morel, I., V. Abalea, P. Cillard J. Cillard (2001) Repair of oxidized DNA by the flavonoid myricetin. Methods Enzymol. 335, 308 316.
31. Wani, A. A., R. E. Gibson-D'Ambrosio S. M. D'Ambrosio (1984) Antibodies to UV irradiated DNA: The monitoring of DNA damage by ELISA and indirect immunofluorescence. Photochem. Photobiol. 40, 465 471.
32. Wani, A. A., S. M. D'Ambrosio N. K. Alvi (1987) Quantitation of pyrimidine dimers by immunoslot blot following sublethal UV-irradiation of human cells. Photochem. Photobiol. 46, 477 482.
33. Wang, Q., Q. Zhu, M. A. Wani, G. Wani, J. Chen A. A. Wani (2003) Tumor suppressor p53 dependent recruitment of nucleotide excision repair factors XPC and TFIIH to DNA damage. DNA Repair 2, 483 499.
34. Sitailo, L. A., S. S. Tibudan M. F. Denning (2002) Activation of caspase-9 is required for UV-induced apoptosis of human keratinocytes. J. Biol. Chem. 277, 19346 19352.
35. Cory, S. J. M. Adams (2002) The Bcl2 family: Regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2, 647 656.
36. Hu, Y., M. A. Benedict, D. Wu, N. Inohara G. Nunez (1998) Bcl-XL interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc. Natl Acad. Sci. USA 95, 4386 4391.
37. Baliga, M. S. S. K. Katiyar (2006) Chemoprevention of photocarcinogenesis by selected dietary botanicals. Photochem. Photobiol. Sci. 5, 243 253.
38. Katiyar, S. K. H. Mukhtar (2001) Green tea polyphenol (-)-epigallocatechin-3-gallate treatment to mouse skin prevents UVB-induced infiltration of leukocytes, depletion of antigen-presenting cells, and oxidative stress. J. Leukoc. Biol. 69, 719 726.
39. Mittal, A., C. A. Elmets S. K. Katiyar (2003) Dietary feeding of proanthocyanidins from grape seeds prevents photocarcinogenesis in SKH-1 hairless mice: Relationship to decreased fat and lipid peroxidation. Carcinogenesis 24, 1379 1388.
40. Herzinger, T., J. O. Funk, K. Hillmer, D. Eick, D. A. Wolf P. Kind (1995) Ultraviolet B irradiation-induced G2 cell cycle arrest in human keratinocytes by inhibitory phosphorylation of the cdc2 cell cycle kinase. Oncogene 11, 2151 2156.
41. Caldwell, M. M., R. Robberecht S. D. Flint (1983) Internal filters: Prospects for UV-acclimation in higher plants. Physiol. Plant 58, 445 450.
42. Boukamp, P., R. T. Petrussevska, D. Breitkreutz, J. Hornung, A. Markham N. E. Fusenig (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106, 761 771.
43. Catani, M. V., A. Rossi, A. Costanzo, S. Sabatini, M. Levrero, G. Melino L. Avigliano (2001) Induction of gene expression via activator protein-1 in the ascorbate protection against UV-induced damage. Biochem. J. 356, 77 85.
44. Phillipson, R. P., S. E. Tobi, J. A. Morris T. J. McMillan (2002) UV-A induces persistent genomic instability in human keratinocytes through an oxidative stress mechanism. Free Radic. Biol. Med. 32, 474 480.
45. Dhanalakshmi, S., G. U. Mallikarjuna, R. P. Singh R. Agarwal (2004) Dual efficacy of silibinin in protecting or enhancing ultraviolet B radiation-caused apoptosis in HaCaT human immortalized keratinocytes. Carcinogenesis 25, 99 106.
46. Reagan-Shaw, S., J. Breur N. Ahmad (2006) Enhancement of UVB radiation-mediated apoptosis by sanguinarine in HaCaT human immortalized keratinocytes. Mol. Cancer Ther. 5, 418 429.
47. Lee, E. R., Y. J. Kang, J. H. Kim, H. T. Lee S. G. Cho (2005) Modulation of apoptosis in HaCaT keratinocytes via differential regulation of ERK signaling pathway by flavonoids. J. Biol. Chem. 280, 31498 31507.
48. Lee, E. R., J. H. Kim, Y. J. Kang S. G. Cho (2007) The anti-apoptotic and anti-oxidant effect of eriodictyol on UV-induced apoptosis in keratinocytes. Biol. Pharm. Bull. 30, 32 37.
49. Afaq, F., D. N. Syed, A. Malik, N. Hadi, S. Sarfaraz, M. H. Kweon, N. Khan, M. A. Zaid H. Mukhtar (2007) Delphinidin, an anthocyanidin in pigmented fruits and vegetables, protects human HaCaT keratinocytes and mouse skin against UVB-mediated oxidative stress and apoptosis. J. Invest. Dermatol. 127, 222 232.
50. Rodriguez-Villanueva, J., D. Greenhalgh, X. J. Wang, D. Bundman, S. Cho, M. Delehedde, D. Roop T. J. McDonnell (1998) Human keratin-1.bcl-2 transgenic mice aberrantly express keratin 6, exhibit reduced sensitivity to keratinocyte cell death induction, and are susceptible to skin tumor formation. Oncogene 16, 853 863.
51. Pena, J. C., E. Fuchs C. B. Thompson (1997) Bcl-x expression influences keratinocyte cell survival but not terminal differentiation. Cell Growth Differ. 8, 619 629.
52. Gillardon, F., I. Moll, M. Meyer T. M. Michaelidis (1999) Alterations in cell death and cell cycle progression in the UV-irradiated epidermis of bcl-2-deficient mice. Cell Death Differ. 6, 55 60.
53. Ricci, J. E., R. A. Gottlieb D. R. Green (2003) Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J. Cell Biol. 160, 65 75.
54. Bernardi, R., C. Negri, M. Donzelli, F. Guano, M. Torti, E. Prosperi A. I. Scovassi (1995) Activation of poly(ADP-ribose)polymerase in apoptotic human cells. Biochimie 77, 378 384.
55. de Laat, A., M. van Tilburg, J. C. van der Leun, W. A. van Vloten F. R. de Gruijl (1996) Cell cycle kinetics following UVA irradiation in comparison to UVB and UVC irradiation. Photochem. Photobiol. 63, 492 497.
56. Petrocelli, T., R. Poon, D. J. Drucker, J. M. Slingerland C. F. Rosen (1996) UVB radiation induces p21Cip1/WAF1 and mediates G1 and S phase checkpoints. Oncogene 12, 1387 1396.
57. Latonen, L., Y. Taya M. Laiho (2001) UV-radiation induces dose-dependent regulation of p53 response and modulates p53-HDM2 interaction in human fibroblasts. Oncogene 20, 6784 6793.
58. Murray, A. W. (1992) Creative blocks: Cell-cycle checkpoints and feedback controls. Nature 359, 599 604.
59. Morgan, D. O. (1995) Principles of CDK regulation. Nature 374, 131 134.
60. Herzinger, T., D. A. Wolf, D. Eick P. Kind (1995) The pRb-related protein p130 is a possible effector of transforming growth factor beta 1 induced cell cycle arrest in keratinocytes. Oncogene 10, 2079 2084.
61. Girard, F., U. Strausfeld, A. Fernandez N. J. Lamb (1991) Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell 67, 1169 1179.
62. Lehner, C. F. P. H. O'Farrell (1989) Expression and function of Drosophila cyclin A during embryonic cell cycle progression. Cell 56, 957 968.
63. Walker, D. H. J. L. Maller (1991) Role for cyclin A in the dependence of mitosis on completion of DNA replication. Nature 354, 314 317.
64. Sancar, A., L. A. Lindsey-Boltz, K. Unsal-Kacmaz S. Linn (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73, 39 85.
65. Placzek, M., S. Gaube, U. Kerkmann, K. P. Gilbertz, T. Herzinger, E. Haen B. Przybilla (2005) Ultraviolet B-induced DNA damage in human epidermis is modified by the antioxidants ascorbic acid and D-alpha-tocopherol. J. Invest. Dermatol. 124, 304 307.
66. Dhanalakshmi, S., G. U. Mallikarjuna, R. P. Singh R. Agarwal (2004) Silibinin prevents ultraviolet radiation-caused skin damages in SKH-1 hairless mice via a decrease in thymine dimer positive cells and an up-regulation of p53-p21/Cip1 in epidermis. Carcinogenesis 25, 1459 1465.
67. Park, C. H., M. J. Lee, J. P. Kim, I. D. Yoo J. H. Chung (2006) Prevention of UV radiation-induced premature skin aging in hairless mice by the novel compound Melanocin A. Photochem. Photobiol. 82, 574 578.
68. Feng, Z., W. Hu, L. J. Marnett M. S. Tang (2006) Malondialdehyde, a major endogenous lipid peroxidation product, sensitizes human cells to UV- and BPDE-induced killing and mutagenesis through inhibition of nucleotide excision repair. Mutat. Res. 601, 125 136.