Protective role of vitamin D signaling in skin cancer formation

Journal of Steroid Biochemistry and Molecular Biology

Volumn 136, Issue 1, 2013, Pages 271-279

  Bikle, Daniel D ^a   Elalieh, Hashem ^a   Welsh, Joellen ^b   Oh, Dennis ^a   Cleaver, James ^a   Teichert, Arnaud ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

1,25 Dihydroxyvitamin D; DNA damage repair; Keratinocyte; Sonic hedgehog; UVR; Vitamin D receptor

Indexed keywords

7,12 DIMETHYLBENZ[A]ANTHRACENE; PROTEIN PATCHED 1; VITAMIN D; VITAMIN D RECEPTOR;

APOPTOSIS; BASAL CELL NEVUS SYNDROME; CANCER CELL CULTURE; CANCER PREVENTION; CELL CYCLE CHECKPOINT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; COCKAYNE SYNDROME; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; EPIDERMIS HYPERPLASIA; EXCISION REPAIR; HUMAN; IONIZING RADIATION; KERATINOCYTE; LONG TERM EXPOSURE; MALIGNANT TRANSFORMATION; OZONE LAYER; REVIEW; SIGNAL TRANSDUCTION; SKIN CANCER; SKIN CARCINOGENESIS; SKIN PROTECTION; SPONTANEOUS MUTATION; ULTRAVIOLET RADIATION; UPREGULATION; VITAMIN BLOOD LEVEL; XERODERMA PIGMENTOSUM;

ANIMALIA; ERINACEIDAE; MUS;

EID: 84881120272     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2012.09.021     Document Type: Review

References (68)

1. J.A. Eisman, T.J. Martin, I. MacIntyre, et al., 1,25-Dihydroxyvitamin-D- receptor in breast cancer cells, Lancet 2 (8156-8157) (1979) 1335-1336.
2. A.V. Ratnam, D.D. Bikle, M.J. Su, et al., Squamous carcinoma cell lines fail to respond to 1,25-dihydroxyvitamin D despite normal levels of the vitamin D receptor, Journal of Investigative Dermatology 106 (3) (1996) 522-525.
3. J. Kamradt, L. Rafi, T. Mitschele, et al., Analysis of the vitamin D system in cutaneous malignancies, Recent Results in Cancer Research 164 (2003) 259-269.
4. K. Colston, M.J. Colston, D. Feldman, 1,25-Dihydroxyvitamin D3 and malignant melanoma: the presence of receptors and inhibition of cell growth in culture, Endocrinology 108 (3) (1981) 1083-1086.
5. C. Garland, R.B. Shekelle, E. Barrett-Connor, et al., Dietary vitamin D and calcium and risk of colorectal cancer: a 19-year prospective study in men, Lancet 1 (8424) (1985) 307-309.
6. R.M. Bostick, J.D. Potter, T.A. Sellers, et al., Relation of calcium, vitamin D, and dairy food intake to incidence of colon cancer among older women. The Iowa Women's Health Study, American Journal of Epidemiology 137 (12) (1993) 1302-1317.
7. J. Kearney, E. Giovannucci, E.B. Rimm, et al., Calcium, vitamin D, and dairy foods and the occurrence of colon cancer in men, American Journal of Epidemiology 143 (9) (1996) 907-917.
8. F.C. Garland, C.F. Garland, E.D. Gorham, et al., Geographic variation in breast cancer mortality in the United States: a hypothesis involving exposure to solar radiation, Preventive Medicine 19 (6) (1990) 614-622.
9. C.L. Hanchette, G.G. Schwartz, Geographic patterns of prostate cancer mortality. Evidence for a protective effect of ultraviolet radiation, Cancer 70 (12) (1992) 2861-2869.
10. R.M. van Dam, Z. Huang, E. Giovannucci, et al., Diet and basal cell carcinoma of the skin in a prospective cohort of men, American Journal of Clinical Nutrition 71 (1) (2000) 135-141.
11. D.J. Hunter, G.A. Colditz, M.J. Stampfer, et al., Diet and risk of basal cell carcinoma of the skin in a prospective cohort of women, Annals of Epidemiology 2 (3) (1992) 231-239.
12. M.A. Weinstock, M.J. Stampfer, R.A. Lew, et al., Case-control study of melanoma and dietary vitamin D: implications for advocacy of sun protection and sunscreen use, Journal of Investigative Dermatology 98 (5) (1992) 809-811.
13. M.M. Asgari, J. Tang, M.E. Warton, et al., Association of prediagnostic serum vitamin D levels with the development of basal cell carcinoma, Journal of Investigative Dermatology 130 (5) (2010) 1438-1443.
14. G.M. Zinser, J.P. Sundberg, J. Welsh, Vitamin D(3) receptor ablation sensitizes skin to chemically induced tumorigenesis, Carcinogenesis 23 (12) (2002) 2103-2109.
15. A.K. Indra, E. Castaneda, M.C. Antal, et al., Malignant transformation of DMBA/TPA-induced papillomas and nevi in the skin of mice selectively lacking retinoid-X-receptor alpha in epidermal keratinocytes, Journal of Investigative Dermatology 127 (5) (2007) 1250-1260.
16. T.I. Ellison, M.K. Smith, A.C. Gilliam, et al., Inactivation of the vitamin D receptor enhances susceptibility of murine skin to UV-induced tumorigenesis, Journal of Investigative Dermatology 128 (2008) 2508-2517.
17. A.E. Teichert, H. Elalieh, P.M. Elias, et al., Overexpression of hedgehog signaling is associated with epidermal tumor formation in vitamin D receptor-null mice, Journal of Investigative Dermatology 131 (11) (2011) 2289-2297.
18. D.D. Bikle, Vitamin D metabolism and function in the skin, Molecular and Cellular Endocrinology 347 (1-2) (2011) 80-89.
19. K.M. Dixon, A.W. Norman, V.B. Sequeira, et al., 1alpha,25(OH)(2)-vitamin D and a nongenomic vitamin D analogue inhibit ultraviolet radiation-induced skin carcinogenesis, Cancer Prevention Research (Philadelphia) 4 (9) (2011) 1485-1494.
20. S.K. Demetriou, K. Ona-Vu, A.E. Teichert, et al., Vitamin D receptor mediates DNA repair and is UV inducible in intact epidermis but not in cultured keratinocytes, Journal of Investigative Dermatology 132 (2012) 2097-2100.
21. M. Aszterbaum, A. Rothman, R.L. Johnson, et al., Identification of mutations in the human PATCHED gene in sporadic basal cell carcinomas and in patients with the basal cell nevus syndrome, Journal of Investigative Dermatology 110 (6) (1998) 885-888.
22. X.L. Ping, D. Ratner, H. Zhang, et al., PTCH mutations in squamous cell carcinoma of the skin, Journal of Investigative Dermatology 116 (4) (2001) 614-616.
23. D.D. Bikle, H. Elalieh, S. Chang, et al., Development and progression of alopecia in the vitamin D receptor null mouse, Journal of Cellular Physiology 207 (2006) 340-353.
24. Y. Oda, M.H. Ishikawa, N.P. Hawker, et al., Differential role of two VDR coactivators, DRIP205 and SRC-3, in keratinocyte proliferation and differentiation, Journal of Steroid Biochemistry and Molecular Biology 103 (3-5) (2007) 776-780.
25. Y. Oda, Y. Uchida, S. Moradian, et al., Vitamin D receptor and coactivators SRC 2 and 3 regulate epidermis-specific sphingolipid production and permeability barrier formation, The Journal of Investigative Dermatology 129 (6) (2009) 1367-1378.
26. A. Besaratinia, T.W. Synold, H.H. Chen, et al., DNA lesions induced by UV A1 and B radiation in human cells: comparative analyses in the overall genome and in the p53 tumor suppressor gene, Proceedings of the National Academy of Sciences of the United States of America 102 (29) (2005) 10058-10063.
27. S.E. Freeman, H. Hacham, R.W. Gange, et al., Wavelength dependence of pyrimidine dimer formation in DNA of human skin irradiated in situ with ultraviolet light, Proceedings of the National Academy of Sciences of the United States of America 86 (14) (1989) 5605-5609.
28. M.R. Hussein, Ultraviolet radiation and skin cancer: molecular mechanisms, Journal of Cutaneous Pathology 32 (3) (2005) 191-205.
29. L. Daya-Grosjean, A. Sarasin, The role of UV induced lesions in skin carcinogenesis: an overview of oncogene and tumor suppressor gene modifications in xeroderma pigmentosum skin tumors, Mutation Research 571 (1-2) (2005) 43-56.
30. A. Ziegler, D.J. Leffell, S. Kunala, et al., Mutation hotspots due to sunlight in the p53 gene of nonmelanoma skin cancers, Proceedings of the National Academy of Sciences of the United States of America 90 (9) (1993) 4216-4220.
31. A. Ziegler, A.S. Jonason, D.J. Leffell, et al., Sunburn and p53 in the onset of skin cancer, Nature 372 (6508) (1994) 773-776.
32. D.E. Brash, J.A. Rudolph, J.A. Simon, et al., A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma, Proceedings of the National Academy of Sciences of the United States of America 88 (22) (1991) 10124-10128.
33. T. Bito, M. Ueda, N.U. Ahmed, et al., Cyclin D and retinoblastoma gene product expression in actinic keratosis and cutaneous squamous cell carcinoma in relation to p53 expression, Journal of Cutaneous Pathology 22 (5) (1995) 427-434.
34. T.D. Tlsty, B.H. Margolin, K. Lum, Differences in the rates of gene amplification in nontumorigenic and tumorigenic cell lines as measured by Luria-Delbruck fluctuation analysis, Proceedings of the National Academy of Sciences of the United States of America 86 (23) (1989) 9441-9445.
35. T.D. Tlsty, Normal diploid human and rodent cells lack a detectable frequency of gene amplification, Proceedings of the National Academy of Sciences of the United States of America 87 (8) (1990) 3132-3136.
36. V.M. Maher, D.J. Dorney, A.L. Mendrala, et al., DNA excision-repair processes in human cells can eliminate the cytotoxic and mutagenic consequences of ultraviolet irradiation, Mutation Research 62 (2) (1979) 311-323.
37. J. Bartkova, N. Rezaei, M. Liontos, et al., Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints, Nature 444 (7119) (2006) 633-637.
38. J.H. Bielas, K.R. Loeb, B.P. Rubin, et al., Human cancers express a mutator phenotype, Proceedings of the National Academy of Sciences of the United States of America 103 (48) (2006) 18238-18242.
39. R.H. Chen, V.M. Maher, J.J. McCormick, Effect of excision repair by diploid human fibroblasts on the kinds and locations of mutations induced by (+/-)-7beta,8 alpha-dihydroxy-9 alpha,10 alpha-epoxy-7,8,9,10- tetrahydrobenzoapyrene in the coding region of the HPRT gene, Proceedings of the National Academy of Sciences of the United States of America 87 (21) (1990) 8680-8684.
40. R.D. Wood, DNA damage recognition during nucleotide excision repair in mammalian cells, Biochimie 81 (1-2) (1999) 39-44.
41. I. Mellon, V.A. Bohr, C.A. Smith, et al., Preferential DNA repair of an active gene in human cells, Proceedings of the National Academy of Sciences of the United States of America 83 (23) (1986) 8878-8882.
42. I. Mellon, G. Spivak, P.C. Hanawalt, Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene, Cell 51 (2) (1987) 241-249.
43. I. Mellon, D.K. Rajpal, M. Koi, et al., Transcription-coupled repair deficiency and mutations in human mismatch repair genes, Science 272 (5261) (1996) 557-560.
44. V.A. Bohr, Gene specific DNA repair, Carcinogenesis 12 (11) (1991) 1983-1992.
45. P.C. Hanawalt, Transcription-coupled repair and human disease, Science 266 (5193) (1994) 1957-1958.
46. J.H. Hoeijmakers, Genome maintenance mechanisms for preventing cancer, Nature 411 (6835) (2001) 366-374.
47. R.D. Wood, M. Mitchell, J. Sgouros, et al., Human DNA repair genes, Science 291 (5507) (2001) 1284-1289.
48. K.M. Dixon, S.S. Deo, G. Wong, et al., Skin cancer prevention: a possible role of 1,25-dihydroxyvitamin D3 and its analogs, Journal of Steroid Biochemistry and Molecular Biology 97 (1-2) (2005) 137-143.
49. R. Gupta, K.M. Dixon, S.S. Deo, et al., Photoprotection by 1,25-dihydroxyvitamin D3 is associated with an increase in p53 and a decrease in nitric oxide products, Journal of Investigative Dermatology 127 (3) (2007) 707-715.
50. P. De Haes, M. Garmyn, H. Degreef, et al., 1,25-Dihydroxyvitamin D3 inhibits ultraviolet B-induced apoptosis, Jun kinase activation, and interleukin-6 production in primary human keratinocytes, Journal of Cellular Biochemistry 89 (4) (2003) 663-673.
51. P.R. Moll, V. Sander, A.M. Frischauf, et al., Expression profiling of vitamin D treated primary human keratinocytes, Journal of Cellular Biochemistry 100 (3) (2007) 574-592.
52. H. Hahn, C. Wicking, P.G. Zaphiropoulous, et al., Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome, Cell 85 (6) (1996) 841-851.
53. M. Aszterbaum, J. Epstein, A. Oro, et al., Ultraviolet and ionizing radiation enhance the growth of BCCs and trichoblastomas in patched heterozygous knockout mice, Nature Medicine 5 (11) (1999) 1285-1291.
54. P.C. Barnfield, X. Zhang, V. Thanabalasingham, et al., Negative regulation of Gli1 and Gli2 activator function by suppressor of fused through multiple mechanisms, Differentiation 73 (8) (2005) 397-405.
55. J. Svard, K. Heby-Henricson, M. Persson-Lek, et al., Genetic elimination of suppressor of fused reveals an essential repressor function in the mammalian hedgehog signaling pathway, Developmental Cell 10 (2) (2006) 187-197.
56. R.L. Johnson, A.L. Rothman, J. Xie, et al., Human homolog of patched, a candidate gene for the basal cell nevus syndrome, Science 272 (5268) (1996) 1668-1671.
57. G. Regl, M. Kasper, H. Schnidar, et al., The zinc-finger transcription factor GLI2 antagonizes contact inhibition and differentiation of human epidermal cells, Oncogene 23 (6) (2004) 1263-1274.
58. G. Regl, M. Kasper, H. Schnidar, et al., Activation of the BCL2 promoter in response to hedgehog/GLI signal transduction is predominantly mediated by GLI2, Cancer Research 64 (21) (2004) 7724-7731.
59. G. Regl, G.W. Neill, T. Eichberger, et al., Human GLI2 and GLI1 are part of a positive feedback mechanism in basal cell carcinoma, Oncogene 21 (36) (2002) 5529-5539.
60. M. Grachtchouk, R. Mo, S. Yu, et al., Basal cell carcinomas in mice overexpressing Gli2 in skin, Nature Genetics 24 (3) (2000) 216-217.
61. M. Nilsson, A.B. Unden, D. Krause, et al., Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1, Proceedings of the National Academy of Sciences of the United States of America 97 (7) (2000) 3438-3443.
62. A.E. Oro, K.M. Higgins, Z. Hu, et al., Basal cell carcinomas in mice overexpressing sonic hedgehog, Science 276 (5313) (1997) 817-821.
63. H. Fan, A.E. Oro, M.P. Scott, et al., Induction of basal cell carcinoma features in transgenic human skin expressing sonic hedgehog, Nature Medicine 3 (7) (1997) 788-792.
64. M. Tojo, T. Mori, H. Kiyosawa, et al., Expression of sonic hedgehog signal transducers, patched and smoothened, in human basal cell carcinoma, Pathology International 49 (8) (1999) 687-694.
65. J.M. Bonifas, S. Pennypacker, P.T. Chuang, et al., Activation of expression of hedgehog target genes in basal cell carcinomas, Journal of Investigative Dermatology 116 (5) (2001) 739-742.
66. T. Eichberger, G. Regl, M.S. Ikram, et al., FOXE1, a new transcriptional target of GLI2 is expressed in human epidermis and basal cell carcinoma, Journal of Investigative Dermatology 122 (5) (2004) 1180-1187.
67. M.F. Bijlsma, C.A. Spek, D. Zivkovic, et al., Repression of smoothened by patcheddependent (pro-)vitamin D3 secretion, PLoS Biology 4 (8) (2006) e232.
68. J.Y. Tang, T.Z. Xiao, Y. Oda, et al., Vitamin D3 inhibits hedgehog signaling and proliferation in murine basal cell carcinomas, Cancer Prevention Research (Philadelphia) 4 (5) (2011) 744-751.