XPC silencing in normal human keratinocytes triggers metabolic alterations through NOX-1 activation-mediated reactive oxygen species

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1807, Issue 6, 2011, Pages 609-619

  Rezvani, Hamid Reza ^a,b,c   Rossignol, Rodrigue ^b,c   Ali, Nsrein ^b,c   Benard, Giovanni ^b,c   Tang, Xiuwei ^a   Yang, Hee Seung ^a   Jouary, Thomas ^d   De Verneuil, Hubert ^b,c   Taïeb, Alain ^b,c,d   Kim, Arianna L ^a   Mazurier, Frédéric ^b,c  

^a Department of Neurology and the Taub Institute for Research on Alzheimer's Disease and the Aging Brain   (United States)

^b INSERM   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d HÔPITAL SAINT ANDRÉ   (France)

Author keywords

Antioxidant enzyme; Genomic stability; Metabolism; NADPH oxidase; ROS; Warburg effect; XPC

Indexed keywords

ADENOSINE TRIPHOSPHATE; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; XERODERMA PIGMENTOSUM GROUP C PROTEIN;

ANTIOXIDANT ACTIVITY; ARTICLE; CELL METABOLISM; CONTROLLED STUDY; ENERGY METABOLISM; GENE OVEREXPRESSION; GENE SILENCING; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; KERATINOCYTE; MALIGNANT TRANSFORMATION; PRIORITY JOURNAL; SQUAMOUS CELL CARCINOMA;

ANTIOXIDANTS; BASE SEQUENCE; CELLS, CULTURED; DNA-BINDING PROTEINS; ENZYME ACTIVATION; HUMANS; KERATINOCYTES; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NADPH OXIDASE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 79955611732     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.12.006     Document Type: Article

References (47)

1. J.E. Cleaver Cancer in xeroderma pigmentosum and related disorders of DNA repair Nat. Rev. Cancer 5 2005 564 573 (Pubitemid 40942832)
2. P.C. Hanawalt Subpathways of nucleotide excision repair and their regulation Oncogene 21 2002 8949 8956 (Pubitemid 36110824)
3. H. van Steeg, and K.H. Kraemer Xeroderma pigmentosum and the role of UV-induced DNA damage in skin cancer Mol. Med. Today 5 1999 86 94 (Pubitemid 29282226)
4. K.H. Kraemer, M.M. Lee, and J. Scotto Xeroderma pigmentosum. Cutaneous, ocular, and neurologic abnormalities in 830 published cases Arch. Dermatol. 123 1987 241 250 (Pubitemid 17002499)
5. M.C. Hollander, R.T. Philburn, A.D. Patterson, S. Velasco-Miguel, E.C. Friedberg, R.I. Linnoila, and A.J. Fornace Jr. Deletion of XPC leads to lung tumors in mice and is associated with early events in human lung carcinogenesis Proc. Natl Acad. Sci. USA 102 2005 13200 13205 (Pubitemid 41325001)
6. L. Miccoli, K.L. Burr, P. Hickenbotham, E.C. Friedberg, J.F. Angulo, and Y.E. Dubrova The combined effects of xeroderma pigmentosum C deficiency and mutagens on mutation rates in the mouse germ line Cancer Res. 67 2007 4695 4699 (Pubitemid 46910175)
7. S.W. Wijnhoven, H.J. Kool, L.H. Mullenders, A.A. van Zeeland, E.C. Friedberg, G.T. van der Horst, H. van Steeg, and H. Vrieling Age-dependent spontaneous mutagenesis in Xpc mice defective in nucleotide excision repair Oncogene 19 2000 5034 5037
8. M. Frechet, E. Warrick, C. Vioux, O. Chevallier, A. Spatz, S. Benhamou, A. Sarasin, F. Bernerd, and T. Magnaldo Overexpression of matrix metalloproteinase 1 in dermal fibroblasts from DNA repair-deficient/cancer-prone xeroderma pigmentosum group C patients Oncogene 27 2008 5223 5232
9. H.R. Rezvani, C. Ged, B. Bouadjar, H. de Verneuil, and A. Taieb Catalase overexpression reduces UVB-induced apoptosis in a human xeroderma pigmentosum reconstructed epidermis Cancer Gene Ther. 15 2008 241 251 (Pubitemid 351367557)
10. H.R. Rezvani, M. Cario-Andre, C. Pain, C. Ged, H. deVerneuil, and A. Taieb Protection of normal human reconstructed epidermis from UV by catalase overexpression Cancer Gene Ther. 14 2007 174 186 (Pubitemid 46110775)
11. H.R. Rezvani, F. Mazurier, M. Cario-Andre, C. Pain, C. Ged, A. Taieb, and H. de Verneuil Protective effects of catalase overexpression on UVB-induced apoptosis in normal human keratinocytes J. Biol. Chem. 281 2006 17999 18007 (Pubitemid 44035599)
12. H.R. Rezvani, W. Mahfouf, N. Ali, C. Chemin, C. Ged, A.L. Kim, H. de Verneuil, A. Taieb, D.R. Bickers, and F. Mazurier Hypoxia-inducible factor-1alpha regulates the expression of nucleotide excision repair proteins in keratinocytes Nucleic Acids Res. 38 2010 797 809
13. G. Benard, B. Faustin, E. Passerieux, A. Galinier, C. Rocher, N. Bellance, J.P. Delage, L. Casteilla, T. Letellier, and R. Rossignol Physiological diversity of mitochondrial oxidative phosphorylation Am. J. Physiol. Cell Physiol. 291 2006 C1172 C1182
14. D.L. Mitchell The relative cytotoxicity of (6-4) photoproducts and cyclobutane dimers in mammalian cells Photochem. Photobiol. 48 1988 51 57
15. K. Bedard, and K.H. Krause The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol. Rev. 87 2007 245 313 (Pubitemid 46209993)
16. W. Chamulitrat, W. Stremmel, T. Kawahara, K. Rokutan, H. Fujii, K. Wingler, H.H. Schmidt, and R. Schmidt A constitutive NADPH oxidase-like system containing gp91phox homologs in human keratinocytes J. Invest. Dermatol. 122 2004 1000 1009 (Pubitemid 38581003)
17. A. Valencia, and I.E. Kochevar Nox1-based NADPH oxidase is the major source of UVA-induced reactive oxygen species in human keratinocytes J. Invest. Dermatol. 128 2008 214 222 (Pubitemid 350249377)
18. M. Brandon, P. Baldi, and D.C. Wallace Mitochondrial mutations in cancer Oncogene 25 2006 4647 4662 (Pubitemid 44187615)
19. J.S. Clerkin, R. Naughton, C. Quiney, and T.G. Cotter Mechanisms of ROS modulated cell survival during carcinogenesis Cancer Lett. 266 2008 30 36
20. R.A. Gatenby, and R.J. Gillies Why do cancers have high aerobic glycolysis? Nat. Rev. Cancer 4 2004 891 899 (Pubitemid 39472955)
21. E. Gottlieb, and I.P. Tomlinson Mitochondrial tumour suppressors: a genetic and biochemical update Nat. Rev. Cancer 5 2005 857 866 (Pubitemid 41746030)
22. S.J. Ralph, S. Rodriguez-Enriquez, J. Neuzil, and R. Moreno-Sanchez Bioenergetic pathways in tumor mitochondria as targets for cancer therapy and the importance of the ROS-induced apoptotic trigger Mol. Aspects Med. 31 2010 29 59
23. L.J. Reitzer, B.M. Wice, and D. Kennell Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells J. Biol. Chem. 254 1979 2669 2676 (Pubitemid 9196102)
24. R. Rossignol, R. Gilkerson, R. Aggeler, K. Yamagata, S.J. Remington, and R.A. Capaldi Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells Cancer Res. 64 2004 985 993 (Pubitemid 38176901)
25. W.J. Koopman, H.J. Visch, J.A. Smeitink, and P.H. Willems Simultaneous quantitative measurement and automated analysis of mitochondrial morphology, mass, potential, and motility in living human skin fibroblasts Cytom. A 69 2006 1 12 (Pubitemid 43062691)
26. W.J. Koopman, H.J. Visch, S. Verkaart, L.W. van den Heuvel, J.A. Smeitink, and P.H. Willems Mitochondrial network complexity and pathological decrease in complex I activity are tightly correlated in isolated human complex I deficiency Am. J. Physiol. Cell Physiol. 289 2005 C881 C890
27. G. Benard, N. Bellance, D. James, P. Parrone, H. Fernandez, T. Letellier, and R. Rossignol Mitochondrial bioenergetics and structural network organization J. Cell Sci. 120 2007 838 848 (Pubitemid 46523485)
28. G. Benard, and R. Rossignol Ultrastructure of the mitochondrion and its bearing on function and bioenergetics Antioxid. Redox Signal. 10 2008 1313 1342
29. H.R. Rezvani, A.L. Kim, R. Rossignol, N. Ali, M. Daly, W. Mahfouf, N. Bellance, A. Taïeb, H. de Verneuil, F. Mazurier, and D.R. Bickers XPC silencing in normal human keratinocytes triggers metabolic alterations that drive the formation of squamous cell carcinomas J. Clin. Invest. 121 2011 195 211
30. O. Warburg On the origin of cancer cells Science 123 1956 309 314
31. J.S. Modica-Napolitano, and K.K. Singh Mitochondria as targets for detection and treatment of cancer Expert Rev. Mol. Med. 4 2002 1 19
32. K. Smolkova, N. Bellance, F. Scandurra, E. Genot, E. Gnaiger, L. Plecita-Hlavata, P. Jezek, and R. Rossignol Mitochondrial bioenergetic adaptations of breast cancer cells to aglycemia and hypoxia J. Bioenerg. Biomembr. 42 2010 55 67
33. N. Bellance, G. Benard, F. Furt, H. Begueret, K. Smolkova, E. Passerieux, J.P. Delage, J.M. Baste, P. Moreau, and R. Rossignol Bioenergetics of lung tumors: alteration of mitochondrial biogenesis and respiratory capacity Int. J. Biochem. Cell Biol. 41 2009 2566 2577
34. S.J. Yeung, J. Pan, and M.H. Lee Roles of p53, MYC and HIF-1 in regulating glycolysis-the seventh hallmark of cancer Cell. Mol. Life Sci. 65 2008 3981 3999
35. H. Pelicano, D. Carney, and P. Huang ROS stress in cancer cells and therapeutic implications Drug Resist. Updat. 7 2004 97 110 (Pubitemid 38736063)
36. N. Ishii, M. Fujii, P.S. Hartman, M. Tsuda, K. Yasuda, N. Senoo-Matsuda, S. Yanase, D. Ayusawa, and K. Suzuki A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes Nature 394 1998 694 697 (Pubitemid 28389798)
37. L.A. Esposito, S. Melov, A. Panov, B.A. Cottrell, and D.C. Wallace Mitochondrial disease in mouse results in increased oxidative stress Proc. Natl Acad. Sci. USA 96 1999 4820 4825 (Pubitemid 29214495)
38. C.Y. Lu, H.C. Lee, H.J. Fahn, and Y.H. Wei Oxidative damage elicited by imbalance of free radical scavenging enzymes is associated with large-scale mtDNA deletions in aging human skin Mutat. Res. 423 1999 11 21
39. M. Berneburg, Y. Kamenisch, and J. Krutmann Repair of mitochondrial DNA in aging and carcinogenesis Photochem. Photobiol. Sci. 5 2006 190 198 (Pubitemid 43228047)
40. Y.H. Wei, and H.C. Lee Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging Exp. Biol. Med. (Maywood) 227 2002 671 682
41. S. Prithivirajsingh, M.D. Story, S.A. Bergh, F.B. Geara, K.K. Ang, S.M. Ismail, C.W. Stevens, T.A. Buchholz, and W.A. Brock Accumulation of the common mitochondrial DNA deletion induced by ionizing radiation FEBS Lett. 571 2004 227 232 (Pubitemid 38992952)
42. K. Adachi, Y. Fujiura, F. Mayumi, A. Nozuhara, Y. Sugiu, T. Sakanashi, T. Hidaka, and H. Toshima A deletion of mitochondrial DNA in murine doxorubicin-induced cardiotoxicity Biochem. Biophys. Res. Commun. 195 1993 945 951 (Pubitemid 23280506)
43. S. Melov, P. Coskun, M. Patel, R. Tuinstra, B. Cottrell, A.S. Jun, T.H. Zastawny, M. Dizdaroglu, S.I. Goodman, T.T. Huang, H. Miziorko, C.J. Epstein, and D.C. Wallace Mitochondrial disease in superoxide dismutase 2 mutant mice Proc. Natl Acad. Sci. USA 96 1999 846 851 (Pubitemid 29072146)
44. M. D'Errico, E. Parlanti, M. Teson, B.M. de Jesus, P. Degan, A. Calcagnile, P. Jaruga, M. Bjoras, M. Crescenzi, A.M. Pedrini, J.M. Egly, G. Zambruno, M. Stefanini, M. Dizdaroglu, and E. Dogliotti New functions of XPC in the protection of human skin cells from oxidative damage EMBO J. 25 2006 4305 4315 (Pubitemid 44435228)
45. J.P. Melis, S.W. Wijnhoven, R.B. Beems, M. Roodbergen, J. van den Berg, H. Moon, E. Friedberg, G.T. van der Horst, J.H. Hoeijmakers, J. Vijg, and H. van Steeg Mouse models for xeroderma pigmentosum group A and group C show divergent cancer phenotypes Cancer Res. 68 2008 1347 1353 (Pubitemid 351346841)
46. S.W. Wijnhoven, E.M. Hoogervorst, H. de Waard, G.T. van der Horst, and H. van Steeg Tissue specific mutagenic and carcinogenic responses in NER defective mouse models Mutat. Res. 614 2007 77 94 (Pubitemid 44909211)
47. D.L. Cheo, L.B. Meira, D.K. Burns, A.M. Reis, T. Issac, and E.C. Friedberg Ultraviolet B radiation-induced skin cancer in mice defective in the Xpc, Trp53, and Apex (HAP1) genes: genotype-specific effects on cancer predisposition and pathology of tumors Cancer Res. 60 2000 1580 1584 (Pubitemid 30183428)