Stage-specific alterations of cyclin expression during UVB-induced murine skin tumor development

Photochemistry and Photobiology

Volumn 75, Issue 1, 2002, Pages 58-67

  Kim, Arianna L ^a   Athar, Mohammad ^a   Bickers, David R ^a   Gautier, Jean ^a  

^a Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN D1; PROTEIN KINASE; PROTEIN P53; CYCLINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; ENZYME ASSAY; EPIDERMIS; FEMALE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUDE MOUSE; PAPILLOMA; PATHOGENESIS; PROTEIN EXPRESSION; SKIN TUMOR; SQUAMOUS CELL CARCINOMA; ULTRAVIOLET B RADIATION; WESTERN BLOTTING; ANIMAL; BIOLOGY; HAIRLESS MOUSE; KERATINOCYTE; METABOLISM; RADIATION EXPOSURE; RADIATION INJURY; ULTRAVIOLET RADIATION;

ANIMALIA; MURINAE; MUS MUSCULUS;

ANIMALS; CYCLIN A; CYCLIN D1; CYCLINS; FEMALE; KERATINOCYTES; MICE; MICE, INBRED HRS; NEOPLASMS, RADIATION-INDUCED; PHOTOBIOLOGY; SKIN NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

EID: 0036371926     PISSN: 00318655     EISSN: None     Source Type: Journal    
DOI: 10.1562/0031-8655(2002)075<0058:SSAOCE>2.0.CO;2     Document Type: Article

References (63)

1. Black, H. S., F. R. deGruijl, P. D. Forbes, J. E. Cleaver, H. N. Ananthaswamy, E. C. deFabo, S. E. Ullrich and R. M. Tyrrell (1997) Photocarcinogenesis: an overview. J. Photochem. Photobiol. B: Biol. 40, 29-47.
2. Sarasin, A. (1999) The molecular pathways of ultraviolet-induced carcinogenesis. Mutat. Res. 428, 5-10.
3. Beehler, B. C., J. Przybyszewski, H. B. Box and M. F. Kulesz-Martin (1992) Formation of 8-hydroxydeoxyguanosine within DNA of mouse keratinocytes exposed in culture to UVB and H202. Carcinogenesis 13, 2003-2007.
4. Harris, C. C. (1996) Structure and function of the p53 tumor suppressor gene: clues for rational cancer therapeutic strategies. J. Natl. Cancer Inst. 88, 1442-1455.
5. Brash, D. E., J. A. Rudolph, J. A. Simon, A. Lin, G. J. McKenna, H. P. Baden, A. J. Halperin and J. Ponten (1991) A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc. Natl. Acad. Sci. USA 88, 10 124-10 128.
6. Brash, D. E., A. Ziegler, A. S. Jonason, J. A. Simon, S. Kunala and D. J. Leffell (1996) Sunlight and sunburn in human skin cancer: p53, apoptosis, and tumor promotion. J. Investig. Dermatol. Symp. Proc. 1, 136-142.
7. Rehman, I., M. Takata, Y. Y. Wu and J. L. Rees (1996) Genetic change in actinic keratoses. Oncogene 12, 2483-2490.
8. Armstrong, B. K., A. Kricker and D. R. English (1997) Sun exposure and skin cancer. Australas. J. Dermatol. 38(Suppl. 1), S1-S6.
9. Ohtsubo, M., A. M. Theodoras, J. Schumacher, J. M. Roberts and M. Pagano (1995) Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol. Cell. Biol. 15, 2612-2624.
10. Hatakeyama, M. and R. A. Weinberg (1995) The role of RB in cell cycle control. Prog. Cell Cycle Res. 1, 9-19.
11. Xu, J., I. B. Gimenez-Conti, J. E. Cunningham, A. M. Collet, M. A. Luna, H. E. Lanfranchi, M. R. Spitz and C. J. Conti (1998) Alterations of p53, cyclin D1, Rb, and H-ras in human oral carcinomas related to tobacco use. Cancer 83, 204-212.
12. Inohara, S., K. Kitagawa and Y. Kitano (1996) Target of skin tumorigenesis: cyclin D1-cdk4. Int. J. Dermatol. 35, 609-613.
13. Zhang, S. Y., S. C. Liu, T. Goodrow, R. Morris and A. J. Klein-Szanto (1997) Increased expression of G1 cyclins and cyclindependent kinases during tumor progression of chemically induced mouse skin neoplasms. Mol. Carcinog. 18, 142-152.
14. Rodriguez-Puebla, M. L., M, LaCava, P. L. Miliani De Marval, J. L. Jorcano, E. R. Richie and C. J. Conti (2000) Cyclin D2 overexpression in transgenic mice induces thymic and epidermal hyperplasia whereas cyclin D3 expression results only in epidermal hyperplasia. Am. J. Pathol. 157, 1039-1050.
15. Robles, A. I., M. L. Rodriguez-Puebla, A. B. Glick, C. Trempus, L. Hansen, P. Sicinski, R. W. Tennant, R. A. Weinberg, S. H. Yuspa and C. J. Conti (1998) Reduced skin tumor development in cyclin D1-deficient mice highlights the oncogenic ras pathway in vivo, Genes Dev. 12, 2469-2474.
16. Fusenig, N. E. and P. Boukamp (1998) Multiple stages and genetic alterations in immortalization, malignant transformation, and tumor progression of human skin keratinocytes. Mol. Carcinog. 23, 144-158.
17. Balasubramanian, S., K. H. Kim, N. Ahmad and H. Mukhtar (1999) Activation of telomerase and its association with G1-phase of the cell cycle during UVB-induced skin tumorigenesis in SKH-1 hairless mouse. Oncogene 18, 1297-1302.
18. Ouhtit, A., H. K. Muller, D. W. Davis, S. E. Ullrich, D. McConkey and H. N. Ananthaswamy (2000) Temporal events in skin injury and the early adaptive responses in ultraviolet-irradiated mouse skin. Am. J. Pathol. 156, 201-207.
19. Berg, R. J., H. J. van Kranen, H. G. Rebel, A. de Vries, W. A. van Vloten, C. F. Van Kreijl, J. C. van der Leun and F. R. de Gruijl (1996) Early p53 alterations in mouse skin carcinogenesis by UVB radiation: immunohistochemical detection of mutant p53 protein in clusters of preneoplastic epidermal cells. Proc. Natl. Acad. Sci. USA 93, 274-278.
20. You, Y. H., P. E. Szabo and G. P. Pfeifer (2000) Cyclobutane pyrimidine dimers form preferentially at the major p53 mutational hotspot in UVB-induced mouse skin tumors. Carcinogenesis 21, 2113-2117.
21. Jiang, W., H. N. Ananthaswamy, H. K. Muller and M. L. Kripke (1999) p53 protects against skin cancer induction by UV-B radiation. Oncogene 18, 4247-4253.
22. Li, G., V. Tron and V. Ho (1998) Induction of squamous cell carcinoma in p53-deficient mice after ultraviolet irradiation. J. Investig. Dermatol. 110, 72-75.
23. Kemp, C. J., L. A. Donehower, A. Bradley and A. Balmain (1993) Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumors. Cell 74, 813-822.
24. Rodriguez-Puebla, M. L., M. LaCava, I. B. Gimenez-Conti, D. G. Johnson and C. J. Conti (1998) Deregulated expression of cell-cycle proteins during premalignant progression in SENCAR mouse skin. Oncogene 17, 2251-2258.
25. Tron, V. A., M. J. Trotter, L. Tang, M. Krajewska, J. C. Reed, V. C. Ho and G. Li (1998) p53-regulated apoptosis is differentiation dependent in ultraviolet B-irradiated mouse keratinocytes. Am. J. Pathol. 153, 579-585.
26. Petrocelli, T., R. Poon, D. J. Drucker, J. M. Slingerland and C. F. Rosen (1996) UVB radiation induces p21Cip1/WAF1 and mediates GI and S phase checkpoints. Oncogene 12, 1387-1396.
27. Kim, A. L., M. Athar, D. R. Bickers and J. Gautier (2000) Ultraviolet B (UVB)-induced G1 arrest is mediated by down-regulation of cyclin-dependent kinase 4 (CDK4) in skin carcinoma cells lacking p53. Proc. Am. Cancer Res. 41, 248.
28. Athar, M., A. L. Kim, N. Ahmad, H. Mukhtar, J. Gautier and D. R. Bickers (2000) Mechanism of ultraviolet B-induced cell cycle arrest in G2/M phase in immortalized skin keratinocytes with defective p53. Biochem. Biophys. Res. Commun. 277, 107-111.
29. Haupt, Y., R. Maya, A. Kazaz and M. Oren (1997) Mdm2 promotes the rapid degradation of p53, Nature 387, 296-299.
30. Sigal, A. and V. Rotter (2000) Oncogenic mutations of the p53 tumor suppressor: the demons of the guardian of the genome. Cancer Res. 60, 6788-6793.
31. Geary, W. A. and P. H. Cooper (1992) Proliferating cell nuclear antigen (PCNA) in common epidermal lesions. An immunohistochemical study of proliferating cell populations. J. Cutan. Pathol. 19, 458-468.
32. Shivji, K. K., M. K. Kenny and R. D. Wood (1992) Proliferating cell nuclear antigen is required for DNA excision repair. Cell 69, 367-374.
33. Limoli, C. L., E. Giedzinski, W. F. Morgan and J. E. Cleaver (2000) Inaugural article: polymerase eta deficiency in the xeroderma pigmentosum variant uncovers an overlap between the S phase checkpoint and double-strand break repair. Proc. Natl. Acad. Sci. USA 97, 7939-7946.
34. Lu, S., J. Tiekso, S. Hietanen, K. Syrjanen, V. K. Havu and S. Syrjanen (1999) Expression of cell-cycle proteins p53, p21 (WAF-1), PCNA and Ki-67 in benign, premalignant and malignant skin lesions with implicated HPV involvement. Acta Dermato-Venereol. 79, 268-273.
35. Athar, M., J. R. Lloyd, D. R. Bickers and H. Mukhtar (1989) Malignant conversion of UV radiation and chemically induced mouse skin benign tumors by free-radical-generating compounds. Carcinogenesis 10, 1841-1845.
36. Athar, M., R. Agarwal, Z. Y. Wang, J. R. Lloyd, D. R. Bickers and H. Mukhtar (1991) All-trans retinoic acid protects against conversion of chemically induced and ultraviolet B radiation-induced skin papillomas to carcinomas. Carcinogenesis 12, 2325-2329.
37. Bickers, D. R. and M. Athar (2000) Novel approaches to chemoprevention of skin cancer. J. Dermatol. 27, 691-695.
38. Zhao, J., X. Jin, E. Yaping, Z. S. Zheng, Y. J. Zhang, M. Athar, V. A. DeLeo, H. Mukhtar, D. R. Bickers and Z. Y. Wang (1999) Photoprotective effect of black tea extracts against UVB-induced phototoxicity in skin. Photochem. Photobiol. 70, 637-644.
39. Lu. Y. P., Y. R. Lou, P. Yen, D. Mitchell, M. T. Huang and A. H. Conney (1999) Time course for early adaptive responses to ultraviolet B light in the epidermis of SKH-1 mice. Cancer Res. 59, 4591-4602.
40. Makinen, M. and F. Stenback (1998) Skin tumor development and keratin expression in different experimental models. Relation to inducing agent and target tissue structure. Exp. Toxicol. Pathol. 50, 199-208.
41. Einspahr, J. G., D. S. Alberts, J. A. Warneke, P. Bozzo, J. Basye, T. M. Grogan, M. A. Nelson and G. T. Bowden (1999) Relationship of p53 mutations to epidermal cell proliferation and apoptosis in human UV-induced skin carcinogenesis. Neoplasia 1, 468-475.
42. Onodera, H., S. Nakamura and T. Sugai (1996) Cell proliferation and p53 protein expressions in cutaneous epithelial neoplasms. Am. J. Dermatopathol. 18, 580-588.
43. Soufir, N., J. P. Moles, C. Vilmer, C. Moch, O. Verola, J. Rivet, A. Tesniere, L. Dubertret and N. Basset-Seguin (1999) P16 UV mutations in human skin epithelial tumors. Oncogene 18, 5477-5481.
44. Brown, K. and A. Balmain (1995) Transgenic mice and squamous multistage skin carcinogenesis. Cancer Metastasis Rev 14, 113-124.
45. Nakazawa, H., D. English, P. L. Randell, K. Nakazawa, N. Martel, B. K. Armstrong and H. Yamasaki (1994) UV and skin cancer: specific p53 gene mutation in normal skin as a biologically relevant exposure measurement. Proc. Natl. Acad. Sci. USA 91, 360-364.
46. Ziegler, A., A. S. Jonason, D. J. Leffell, J. A. Simon, H. W. Sharma, J. Kimmelman, L. Remington, T. Jacks and D. E. Brash (1994) Sunburn and p53 in the onset of skin cancer. Nature 372, 773-776.
47. Urano, Y., T. Asano, K. Yoshimoto, H. Iwahana, Y. Kubo, S. Kato, S. Sasaki, N. Takeuchi, N. Uchida, H. Nakanishi (1995) Frequent p53 accumulation in the chronically sun-exposed epidermis and clonal expansion of p53 mutant cells in the epidermis adjacent to basal cell carcinoma. J. Investig. Dermatol. 104, 928-932.
48. Macleod, K. F. and T. Jacks (1999) Insights into cancer from transgenic mouse models. J. Pathol. 187, 43-60.
49. Arber, N., C. Lightdale, H. Rotterdam, K. H. Han, A. Sgambato, E. Yap, H. Ahsan, J. Finegold, P. D. Stevens, P. H. Green, H. Hibshoosh, A. I. Neugut, P. R. Holt and I. B. Weinstein (1996) Increased expression of the cyclin D1 gene in Barrett's esophagus. Cancer Epidemiol. Biomark. Prev. 5, 457-459.
50. Arber, N., T. Sutter, M. Miyake, S. M. Kahn, V. S. Venkatraj, A. Sobrino, D. Warburton, P. R. Holt and I. B. Weinstein (1996) Increased expression of cyclin D1 and the Rb tumor suppressor gene in c- K-ras transformed rat enterocytes. Oncogene 12, 1903-1908.
51. Donnellan. R. and R. Chetty (1998) Cyclin DI and human neoplasia. Mol. Pathol. 51, 1-7.
52. Frierson, H. F., Jr., M. J. Gaffey, L. R. Zukerberg, A. Arnold and M. E. Williams (1996) Immunohistochemical detection and gene amplification of cyclin D1 in mammary infiltrating ductal carcinoma. Mod. Pathol. 9, 725-730.
53. Michalides, R., N. van Veelen, A. Hart, B. Loftus, E. Wientjens and A. Balm (1995) Overexpression of cyclin DI correlates with recurrence in a group of forty-seven operable squamous cell carcinomas of the head and neck. Cancer Res. 55, 975-978.
54. Robles, A. I., F. Larcher, R. B. Whalin, R. Murillas, E. Richie, I. B. Gimenez-Conti, J. L. Jorcano and C. J. Conti (1996) Expression of cyclin D1 in epithelial tissues of transgenic mice results in epidermal hyperproliferation and severe thymic hyperplasia. Proc. Natl. Acad. Sci. USA 93, 7634-7638.
55. Liang, S. B., M. Furihata, T. Takeuchi, J. Iwata, B. K. Chen, H. Sonobe and Y. Ohtsuki (2000) Overexpression of cyclin D1 in nonmelanocytic skin cancer. Virchows Arch. 436, 370-376.
56. Bito, T., M. Ueda, N. U. Ahmed, T. Nagano and M. Ichihashi (1995) Cyclin D and retinoblastoma gene product expression in actinic keratosis and cutaneous squamous cell carcinoma in relation to p53 expression. J. Cutan. Pathol. 22, 427-434.
57. Robles, A. I. and C. J. Conti (1995) Early overexpression of cyclin D1 protein in mouse skin carcinogenesis. Carcinogenesis 16, 781-786.
58. Gangarosa, L. M., N. Sizemore, R. Graves-Deal, S. M. Oldham, C. J. Der and R. J. Coffey (1997) A raf-independent epidermal growth factor receptor autocrine loop is necessary for Ras transformation of rat intestinal epithelial cells. J. Biol. Chem. 272, 18 926-18 931.
59. Rodriguez-Puebla, M. L., A. I. Robles and C. J. Conti (1999) ras activity and cyclin D1 expression: an essential mechanism of mouse skin tumor development. Mol. Carcinog. 24, 1-6.
60. Dutta, A., R. Chandra, L. M. Leiter and S. Lester (1995) Cyclins as markers of tumor proliferation: immunocytochemical studies in breast cancer. Proc. Natl. Acad. Sci. USA 92, 5386-5390.
61. Haddad, R., A. D. Morrow, C. Plass and W. A. Held (2000) Restriction landmark genomic scanning of mouse liver tumors for gene amplification: overexpression of cyclin A2. Biochem. Biophys. Res. Commun. 274, 188-196.
62. Volm, M., R. Koomagi, J. Mattern and G. Stammler (1997) Cyclin A is associated with an unfavourable outcome in patients with non-small-cell lung carcinomas. Br. J. Cancer 75, 1774-1778.
63. Lotayef, M., G. D. Wilson, F. M. Daley, H. K. Awwad and T. Shouman (2000) Aberrant expression of cyclin A in head and neck cancer. Br. J. Cancer 83, 30-34.