Resveratrol-sensitized UVA induced apoptosis in human keratinocytes through mitochondrial oxidative stress and pore opening

Journal of Photochemistry and Photobiology B: Biology

Volumn 113, Issue , 2012, Pages 42-50

  Boyer, Jean Z ^a,b,d   Jandova, Jana ^a,b,d   Janda, Jaroslav ^a,b,d   Vleugels, Frank R ^b   Elliott, David A ^c   Sligh, James E ^a,b,d  

^a SOUTHERN ARIZONA VA HEALTH CARE SYSTEM   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF ARIZONA   (United States)

Author keywords

Keratinocyte; Mitochondrial membrane potential; Mitochondrial permeability transition pore; Reactive oxygen species; Resveratrol; UVA induced apoptosis

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 2; PROTEIN BCL 2; RESVERATROL;

APOPTOSIS; ARTICLE; BLUEBERRY; CANCER GROWTH; CELL CYCLE ARREST; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; CRANBERRY; DOWN REGULATION; HEART PROTECTION; HUMAN; HUMAN CELL; KERATINOCYTE; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION; MYELOMA CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; SENSITIZATION; SKIN TUMOR; ULTRAVIOLET A RADIATION;

APOPTOSIS; HEK293 CELLS; HUMANS; KERATINOCYTES; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; OXIDATIVE STRESS; STILBENES; ULTRAVIOLET RAYS;

VACCINIUM; VITACEAE;

EID: 84862234322     PISSN: 10111344     EISSN: 18732682     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2012.04.013     Document Type: Article

References (48)

1. W.M. Olsen, H.S. Huitfeldt, and G. Eggset UVB-induced (6-4) photoproducts in hairless mouse epidermis studied by quantitative immunohistochemistry Carcinogenesis 10 1989 1669 1673 (Pubitemid 19222267)
2. F. Bernerd, and D. Asselineau Successive alteration and recovery of epidermal differentiation and morphogenesis after specific UVB-damages in skin reconstructed in vitro Dev. Biol. 183 1997 123 138 (Pubitemid 27148642)
3. M. Ming, W. Han, J. Maddox, K. Soltani, C.R. Shea, D.M. Freeman, and Y.Y. He UVB-induced ERK/AKT-dependent PTEN suppression promotes survival of epidermal keratinocytes Oncogene 29 2010 492 502
4. M.S. Cooke, N. Mistry, A. Ladapo, K.E. Herbert, and J. Lunec Immunochemical quantitation of UV-induced oxidative and dimeric DNA damage to human keratinocytes Free Radic. Res. 33 2000 369 381
5. G.F. Vile, A. Tanew-Ilitschew, and R.M. Tyrrell Activation of NF-kappa B in human skin fibroblasts by the oxidative stress generated by UVA radiation Photochem. Photobiol. 62 1995 463 468
6. E. Strozyk, B. Poppelmann, T. Schwarz, and D. Kulms Differential effects of NF-kappaB on apoptosis induced by DNA-damaging agents: the type of DNA damage determines the final outcome Oncogene 25 2006 6239 6251 (Pubitemid 44564741)
7. X.X. Huang, F. Bernerd, and G.M. Halliday Ultraviolet a within sunlight induces mutations in the epidermal basal layer of engineered human skin Am. J. Pathol. 174 2009 1534 1543
8. Y.Y. He, J. Pi, J.L. Huang, B.A. Diwan, M.P. Waalkes, and C.F. Chignell Chronic UVA irradiation of human HaCaT keratinocytes induces malignant transformation associated with acquired apoptotic resistance Oncogene 25 2006 3680 3688 (Pubitemid 43980489)
9. S. Tada-Oikawa, S. Oikawa, and S. Kawanishi Role of ultraviolet A-induced oxidative DNA damage in apoptosis via loss of mitochondrial membrane potential and caspase-3 activation Biochem. Biophys. Res. Commun. 247 1998 693 696 (Pubitemid 28418453)
10. M. Djavaheri-Mergny, C. Marsac, C. Maziere, R. Santus, L. Michel, L. Dubertret, and J.C. Maziere UV-A irradiation induces a decrease in the mitochondrial respiratory activity of human NCTC 2544 keratinocytes Free Radic. Res. 34 2001 583 594 (Pubitemid 32694647)
11. D. Delmas, A. Lancon, D. Colin, B. Jannin, and N. Latruffe Resveratrol as a chemopreventive agent: a promising molecule for fighting cancer Curr. Drug Targets 7 2006 423 442 (Pubitemid 43744833)
12. J.K. Kundu, Y.K. Shin, S.H. Kim, and Y.J. Surh Resveratrol inhibits phorbol ester-induced expression of COX-2 and activation of NF-kappaB in mouse skin by blocking IkappaB kinase activity Carcinogenesis 27 2006 1465 1474 (Pubitemid 43994860)
13. T.A. Zykova, F. Zhu, X. Zhai, W.Y. Ma, S.P. Ermakova, K.W. Lee, A.M. Bode, and Z. Dong Resveratrol directly targets COX-2 to inhibit carcinogenesis Mol. Carcinog. 47 2008 797 805
14. V.M. Adhami, F. Afaq, and N. Ahmad Suppression of ultraviolet B exposure-mediated activation of NF-kappaB in normal human keratinocytes by resveratrol Neoplasia 5 2003 74 82 (Pubitemid 36151060)
15. B.B. Aggarwal, A. Bhardwaj, R.S. Aggarwal, N.P. Seeram, S. Shishodia, and Y. Takada Role of resveratrol in prevention and therapy of cancer: preclinical and clinical studies Anticancer Res. 24 2004 2783 2840 (Pubitemid 39409568)
16. Y.J. Surh, Y.J. Hurh, J.Y. Kang, E. Lee, G. Kong, and S.J. Lee Resveratrol, an antioxidant present in red wine, induces apoptosis in human promyelocytic leukemia (HL-60) cells Cancer Lett. 140 1999 1 10 (Pubitemid 29251307)
17. M. Seve, F. Chimienti, S. Devergnas, M. Aouffen, T. Douki, J. Chantegrel, J. Cadet, and A. Favier Resveratrol enhances UVA-induced DNA damage in HaCaT human keratinocytes Med. Chem. 1 2005 629 633
18. P. Boukamp, R.T. Petrussevska, D. Breitkreutz, J. Hornung, A. Markham, and N.E. Fusenig Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line J. Cell. Biol. 106 1988 761 771 (Pubitemid 18089976)
19. K.G. Norman, J.A. Canter, M.J. Shi, G.L. Milne, J.D. Morrow, and J.E. Sligh Cyclosporine A suppresses keratinocyte cell death through MPTP inhibition in a model for skin cancer in organ transplant recipients Mitochondrion 10 2010 94 101
20. J. Cadet, T. Douki, J.L. Ravanat, and P. Di Mascio Sensitized formation of oxidatively generated damage to cellular DNA by UVA radiation Photochem. Photobiol. Sci. 8 2009 903 911
21. P. Morliere, S. Salmon, M. Aubailly, A. Risler, and R. Santus Sensitization of skin fibroblasts to UVA by excess iron Biochim. Biophys. Acta 1334 1997 283 290 (Pubitemid 27117532)
22. F. Afaq, V.M. Adhami, N. Ahmad, and H. Mukhtar Botanical antioxidants for chemoprevention of photocarcinogenesis Front. Biosci. 7 2002 d784 792
23. A. Quincozes-Santos, A.C. Andreazza, P. Nardin, C. Funchal, C.A. Goncalves, and C. Gottfried Resveratrol attenuates oxidative-induced DNA damage in C6 Glioma cells Neurotoxicology 28 2007 886 891 (Pubitemid 47058578)
24. Y. Bai, Q.Q. Mao, J. Qin, X.Y. Zheng, Y.B. Wang, K. Yang, H.F. Shen, and L.P. Xie Resveratrol induces apoptosis and cell cycle arrest of human T24 bladder cancer cells in vitro and inhibits tumor growth in vivo Cancer Sci. 101 2010 488 493
25. A. Kotha, M. Sekharam, L. Cilenti, K. Siddiquee, A. Khaled, A.S. Zervos, B. Carter, J. Turkson, and R. Jove Resveratrol inhibits Src and Stat3 signaling and induces the apoptosis of malignant cells containing activated Stat3 protein Mol. Cancer Ther. 5 2006 621 629
26. L.F. Zheng, Q.Y. Wei, Y.J. Cai, J.G. Fang, B. Zhou, L. Yang, and Z.L. Liu DNA damage induced by resveratrol and its synthetic analogues in the presence of Cu (II) ions: mechanism and structure-activity relationship Free Radic. Biol. Med. 41 2006 1807 1816 (Pubitemid 44839142)
27. S.M. Hadi, M.F. Ullah, A.S. Azmi, A. Ahmad, U. Shamim, H. Zubair, and H.Y. Khan Resveratrol mobilizes endogenous copper in human peripheral lymphocytes leading to oxidative DNA breakage: a putative mechanism for chemoprevention of cancer Pharm. Res. 27 2010 979 988
28. 2 J. Biol. Chem. 266 1991 20175 20184 (Pubitemid 21908442)
29. M.A. Verity, and J.K. Gambell Studies of copper ion-induced mitochondrial swelling in vitro Biochem. J. 108 1968 289 295
30. J.A. Baur, and D.A. Sinclair Therapeutic potential of resveratrol: the in vivo evidence Nat. Rev. Drug Discov. 5 2006 493 506 (Pubitemid 44136961)
31. N. Ahmad, V.M. Adhami, F. Afaq, D.K. Feyes, and H. Mukhtar Resveratrol causes WAF-1/p21-mediated G(1)-phase arrest of cell cycle and induction of apoptosis in human epidermoid carcinoma A431 cells Clin. Cancer Res. 7 2001 1466 1473 (Pubitemid 32708704)
32. C. von Ballmoos, A. Wiedenmann, and P. Dimroth Essentials for ATP synthesis by F1F0 ATP synthases Annu. Rev. Biochem. 78 2009 649 672
33. J. Zheng, and V.D. Ramirez Inhibition of mitochondrial proton F0F1-ATPase/ATP synthase by polyphenolic phytochemicals Br. J. Pharmacol. 130 2000 1115 1123 (Pubitemid 30453547)
34. J. Dorrie, H. Gerauer, Y. Wachter, and S.J. Zunino Resveratrol induces extensive apoptosis by depolarizing mitochondrial membranes and activating caspase-9 in acute lymphoblastic leukemia cells Cancer Res. 61 2001 4731 4739 (Pubitemid 32691883)
35. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress Biochem. J. 255 1988 357 360
36. M.J. Hansson, R. Mansson, G. Mattiasson, J. Ohlsson, J. Karlsson, M.F. Keep, and E. Elmer Brain-derived respiring mitochondria exhibit homogeneous, complete and cyclosporin-sensitive permeability transition J. Neurochem. 89 2004 715 729 (Pubitemid 38534157)
37. S. Malouitre, H. Dube, D. Selwood, and M. Crompton Mitochondrial targeting of cyclosporin A enables selective inhibition of cyclophilin-D and enhanced cytoprotection after glucose and oxygen deprivation Biochem. J. 425 2010 137 148
38. Y.M. Li, N. Johnson, M. Capano, M. Edwards, and M. Crompton Cyclophilin-D promotes the mitochondrial permeability transition but has opposite effects on apoptosis and necrosis Biochem. J. 383 2004 101 109 (Pubitemid 39389455)
39. E. Basso, L. Fante, J. Fowlkes, V. Petronilli, M.A. Forte, and P. Bernardi Properties of the permeability transition pore in mitochondria devoid of Cyclophilin D J. Biol. Chem. 280 2005 18558 18561 (Pubitemid 41379552)
40. T.A. Lehman, R. Modali, P. Boukamp, J. Stanek, W.P. Bennett, J.A. Welsh, R.A. Metcalf, M.R. Stampfer, N. Fusenig, and E.M. Rogan P53 mutations in human immortalized epithelial cell lines Carcinogenesis 14 1993 833 839 (Pubitemid 23169134)
41. K.C. Morris, H.W. Lin, J.W. Thompson, and M.A. Perez-Pinzon Pathways for ischemic cytoprotection: role of sirtuins in caloric restriction, resveratrol, and ischemic preconditioning J. Cereb. Blood Flow. Metab. 31 2011 1003 1019
42. A.P. Raval, H.W. Lin, K.R. Dave, R.A. DeFazio, D. Della Morte, E.J. Kim, and M.A. Perez-Pinzon Resveratrol and ischemic preconditioning in the brain Curr. Med. Chem. 15 2008 1545 1551 (Pubitemid 351997786)
43. D. Delmas, E. Solary, and N. Latruffe Resveratrol, a phytochemical inducer of multiple cell death pathways: apoptosis, autophagy and mitotic catastrophe Curr. Med. Chem. 18 2011 1100 1121
44. T.C. Hsieh, and J.M. Wu Resveratrol: biological and pharmaceutical properties as anticancer molecule Biofactors 36 2010 360 369
45. S.K. Manna, A. Mukhopadhyay, and B.B. Aggarwal Resveratrol suppresses TNF-induced activation of nuclear transcription factors NF-kappaB, activator protein-1, and apoptosis: potential role of reactive oxygen intermediates and lipid peroxidation J. Immunol. 164 2000 6509 6519 (Pubitemid 30408836)
46. A. Kumar, and S.S. Sharma NF-kappaB inhibitory action of resveratrol: a probable mechanism of neuroprotection in experimental diabetic neuropathy Biochem. Biophys. Res. Commun. 394 2010 360 365
47. C.E. Wenner Targeting mitochondria as a therapeutic target in cancer J. Cell. Physiol. 227 2012 450 456
48. F. Schwartzenberg-Bar-Yoseph, M. Armoni, and E. Karnieli The tumor suppressor p53 down-regulates glucose transporters GLUT1 and GLUT4 gene expression Cancer Res. 64 2004 2627 2633 (Pubitemid 38523921)