Topical thymidine dinucleotide application protects against UVB-induced skin cancer in mice with DNA repair gene (Ercc1)-deficient skin

DNA Repair

Volumn 8, Issue 5, 2009, Pages 664-671

  Lawrence, Nicola J ^a   Song, Liang ^a   Doig, Jennifer ^a   Ritchie, Ann Marie ^a   Brownstein, David G ^b   Melton, David W ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

DNA damage; DNA repair; Nucleotide excision repair; Ultraviolet irradiation

Indexed keywords

DINUCLEOTIDE; THYMIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER PREVENTION; CELL PROLIFERATION; CONTROLLED STUDY; DNA REPAIR; EPIDERMIS; ERCC1 GENE; ERYTHEMA; EXCISION REPAIR; GENE; KERATINOCYTE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN CANCER; SKIN CARCINOGENESIS; SURVIVAL TIME; ULTRAVIOLET B RADIATION; ULTRAVIOLET IRRADIATION; ULTRAVIOLET RADIATION; UPREGULATION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CELLS, CULTURED; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; ENDONUCLEASES; EPIDERMIS; ERYTHEMA; FEMALE; IMMUNOENZYME TECHNIQUES; INTEGRASES; KERATINOCYTES; MALE; MICE; MICE, KNOCKOUT; NEOPLASMS, RADIATION-INDUCED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SKIN NEOPLASMS; SURVIVAL RATE; THYMIDINE; ULTRAVIOLET RAYS; WHOLE-BODY IRRADIATION;

ANIMALIA; MUS;

EID: 63649093828     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2009.01.020     Document Type: Article

References (39)

1. Eller M.S., Yaar M., and Gilchrest B.A. DNA damage and melanogenesis. Nature 372 (1994) 413-414
2. Eller M.S., Maeda T., Magnoni C., Atwal D., and Gilchrest B.A. Enhancement of DNA repair in human skin cells by thymidine dinucleotides: evidence for a p53 mediated mammalian SOS response. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 12627-12632
3. Goukassian D.A., Eller M.S., Yaar M., and Gilchrest B.A. Thymidine dinucleotide mimics the effect of solar simulated irradiation of p53 and p53 regulated proteins. J. Invest. Dermatol. 112 (1999) 25-31
4. Goukassian D.A., Bagheri S., El-Keeb L., Eller M.S., and Gilchrest B.A. DNA oligonucleotide treatment corrects the age associated decline in DNA repair activity. FASEB J. 16 (2002) 754-756
5. Cruz Jr. P.D., Leverkus M., Dougherty I., Gleason M.J., Eller M., Yaar M., and Gilchrest B.A. Thymidine dinucleotides inhibit contact hypersensitivity and activate the gene for tumour necrosis factor alpha. J. Invest. Dermatol. 114 (2000) 253-258
6. Curiel-Lewandrowski C., Venna S.S., Eller M.S., Cruikshank W., Dougherty I., Cruz Jr. P.D., and Gilchrest B.A. Inhibition of the elicitation phase of contact hypersensitivity by thymidine dinucleotides is in part mediated by increased expression of interleukin-10 in human keratinocytes. Exp. Dermatol. 12 (2003) 145-152
7. de Lange T. Protection of mammalian telomeres. Oncogene 21 (2002) 532-540
8. Griffith J.D., Comeau L., Rosenfield S., Stansel R.M., Bianchi A., Moss H., and de Lange T. Mammalian telomeres end in a large duplex loop. Cell 97 (1999) 503-514
9. Eller M.S., Puri N., Hadshiew I.M., Venna S.S., and Gilchrest B.A. Induction of apoptosis by telomere 3′ overhang specific DNA. Exp. Cell Res. 276 (2002) 185-193
10. Eller M.S., Li G.Z., Firoozabadi R., Puri N., and Gilchrest B.A. Induction of a p95/Nbs1-mediated S phase checkpoint by telomere 3′ overhang specific DNA. FASEB J. 17 (2003) 152-162
11. Goukassian D.A., Helms E., van Steeg H., van Oostrom C., Bhawan J., and Gilchrest B.A. Topical DNA oligonucleotide therapy reduces UV-induced mutations and photocarcinogenesis in hairless mice. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 3933-3938
12. Goukassian D.A., and Gilchrest B.A. The interdependence of skin aging, skin cancer, and DNA repair capacity: a novel perspective with therapeutic implications. Rejuvenation Res. 7 (2004) 175-185
13. Gillet L.C., and Scharer O.D. Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem. Rev. 106 (2006) 253-276
14. Jaspers N.G., Raams A., Cirillo Silengo M.C., Wijgers N., Niedernhofer L.J., Robinson A.R., Giglia-Mari G., Hoogstraten D., Kleijer W.J., Hoeijmakers J.H., and Vermeulen W. First reported patient with human ERCC1 deficiency has cerebro-oculo-facio-skeletal syndrome with a mild defect in nucleotide excision repair and severe developmental failure. Am. J. Hum. Genet. 80 (2007) 457-466
15. Doig J., Anderson C., Lawrence N.J., Selfridge J., Brownstein D.G., and Melton D.W. Mice with skin-specific DNA repair gene (Ercc1) inactivation are hypersensitive to ultraviolet irradiation-induced skin cancer and show more rapid actinic progression. Oncogene 25 (2006) 6229-6238
16. Ramirez A., Page A., Gandarillas A., Zanet J., Pibre S., Vidal M., Tusell L., Genesca A., Whitaker D.A., Melton D.W., and Jorcano J.L. A keratin K5Cre transgenic line appropriate for tissue specific or generalised Cre mediated recombination. Genesis 39 (2004) 52-57
17. Berg R.J., de Vries A., van Steeg H., and de Gruijl F.R. Relative susceptibilities of XPA knockout mice and their heterozygous and wild-type littermates to UVB-induced skin cancer. Cancer Res. 57 (1997) 581-584
18. de Vries A., Berg R.J., Wijnhoven S., Westerman A., Wester P.W., van Kreijl C.F., Capel P.J., de Gruijl F.R., van Kranen H.J., and van Steeg H. XPA-deficiency in hairless mice causes a shift in skin tumor types and mutational target genes after exposure to low doses of U.V.B. Oncogene 16 (1998) 2205-2212
19. Farr P., and Diffey B.L. Quantitative studies on cutaneous erythema induced by ultraviolet radiation. Br. J. Dermatol. 111 (1984) 673-682
20. Gallagher C.H., Canfield P.J., Greenoak G.E., and Reeve V.E. Characterization and histogenesis of tumors in the hairless mouse produced by low-dosage incremental ultraviolet radiation. J. Invest. Dermatol. 83 (1984) 169-174
21. Canfield P.J., Greenoak G.E., Macasaet E.N., Reeve V.E., and Gallagher C.H. The characterization of squamous cell carcinoma induced by ultraviolet irradiation in hairless mice. Pathology 20 (1988) 109-117
22. Melton D.W., Ketchen A.-M., Nuñez F., Bonatti-Abbondandolo S., Abbondandolo A., Squires S., and Johnson R.T. Cells from ERCC1-deficient mice show increased genome instability and a reduced frequency of S-phase-dependent illegitimate chromosome exchange, but a normal frequency of homologous recombination. J. Cell Sci. 111 (1998) 395-404
23. McWhir J., Selfridge J., Harrison D.J., Squires S., and Melton D.W. Mice with DNA repair gene (ERCC-1) deficiency have elevated levels of p53, liver nuclear abnormalities and die before weaning. Nat. Genet. 5 (1993) 217-224
24. Chipchase M.D., O'Neill M., and Melton D.W. Characterisation of premature liver polyploidy in DNA repair (Ercc1)-deficient mice. Hepatology 38 (2003) 958-966
25. +/- mice. Am. J. Pathol. 172 (2008) 1248-1255
26. Ohashi N., Yaar M., Eller M.S., Truzzi F., and Gilchrest B.A. Features that determine telomere homolog oligonucleotide-induced therapeutic DNA damage-like responses in cancer cells. J. Cell. Physiol. 210 (2007) 582-595
27. Yaar M., Eller M.S., Panova I., Kubera J., Wee L.H., Cowan K.H., and Gilchrest B.A. Telomeric DNA induces apoptosis and senescence of human breast carcinoma cells. Breast Cancer Res. 9 (2007) R13
28. Pedeux R., Al-Irani N., Marteau C., Pellicier F., Branche R., Ozturk M., Franchi J., and Dore J.F. Thymidine dinucleotides induce S phase cell cycle arrest in addition to increased melanogenesis in human melanocytes. J. Invest. Dermatol. 111 (1998) 472-477
29. Puri N., Eller M.S., Byers H.R., Dykstra S., Kubera J., and Gilchrest B.A. Telomere based DNA damage responses: a new approach to melanoma. FASEB J. 18 (2004) 1373-1381
30. Aziz M.H., Reagan-Shaw S., Wu J., Longley B.J., and Ahmad N. Chemoprevention of skin cancer by grape constituent resveratrol: relevance to human disease?. FASEB J. 19 (2005) 1193-1195
31. Mallikarjuna G., Dhanalakshmi S., Singh R.P., Agarwal C., and Agarwal R. Silibinin protects against photocarcinogenesis via modulation of cell cycle regulators, mitogen-activated protein kinases, and Akt signaling. Cancer Res. 64 (2004) 6349-6356
32. Dhanalakshmi S., Agarwal C., Singh R.P., and Agarwal R. Silibinin up-regulates DNA-protein kinase-dependent p53 activation to enhance UVB-induced apoptosis in mouse epithelial JB6 cells. J. Biol. Chem. 280 (2005) 20375-20383
33. Lu Y.P., Lou Y.R., Xie J.G., Peng Q.Y., Zhou S., Lin Y., Shih W.J., and Conney A.H. Caffeine and caffeine sodium benzoate have a sunscreen effect, enhance UVB-induced apoptosis, and inhibit UVB-induced skin carcinogenesis in SKH-1 mice. Carcinogenesis 28 (2007) 199-206
34. Bair W.B., Hart III N., Einspahr J., Liu G., Dong Z., Alberts D., and Bowden G.T. Inhibitory effects of sodium salicylate and acetylsalicylic acid on UVB-induced mouse skin carcinogenesis. Cancer Epidemiol. Biomarkers Prev. 11 (2002) 1645-1652
35. Petersen A.B., Na R., and Wulf H.C. Sunless skin tanning with dihydroxyacetone delays broad-spectrum ultraviolet photocarcinogenesis in hairless mice. Mutat. Res. 542 (2003) 129-138
36. Kripke M.L., Cox P.A., Alas L.G., and Yarosh D.B. Pyrimidine dimers in DNA initiate systemic immunosuppression in UV-irradiated mice. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 7516-7520
37. Nishigori C., Yarosh D.B., Ullrich S.E., Vink A.A., Bucana C.D., Roza L., and Kripke M.L. Evidence that DNA damage triggers interleukin-10 cytokine production in UV-irradiated murine keratinocytes. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 10354-10359
38. Yarosh D., Klein J., O'Connor A., Hawk J., Rafal E., and Wolf P. Effect of topically applied T4 endonuclease V in liposomes on skin cancer in xeroderma pigmentosum: a randomised study. Lancet 357 (2001) 926-929
39. Lucas R.M., Repacholi M.H., and McMichael A.J. Is the current public health message on UV exposure correct?. Bull. World Health Org. 84 (2006) 485-491