p53 prevents progression of nevi to melanoma predominantly through cell cycle regulation

Pigment Cell and Melanoma Research

Volumn 23, Issue 6, 2010, Pages 781-794

  Terzian, Tamara ^a   Torchia, Enrique C ^a   Dai, Daisy ^a   Robinson, Steven E ^a   Murao, Kazutoshi ^a   Stiegmann, Regan A ^a   Gonzalez, Victoria ^a   Boyle, Glen M ^b   Powell, Marianne B ^c   Pollock, Pamela M ^d   Lozano, Guillermina ^e   Robinson, William A ^a   Roop, Dennis R ^a   Box, Neil F ^a  

^a UC Denver   (United States)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^c STANFORD UNIVERSITY   (United States)

^d TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Mdm4; Melanoma; Nevus; Nutlin 3; P21; P53; Progression

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; DIMETHYLBENZ[A]ANTHRACENE; NUTLIN 3; PROTEIN P53;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CELL AGING; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL VIABILITY; CLONOGENESIS; GENE ACTIVATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; MALIGNANT TRANSFORMATION; MELANOCYTE; MELANOGENESIS; MELANOMA; MELANOMA CELL; METASTASIS; MOUSE; NEVUS; NONHUMAN; ONSET AGE; OVERALL SURVIVAL; SKIN CARCINOGENESIS; TUMOR SUPPRESSOR GENE;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; CELL AGING; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CLONE CELLS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HUMANS; IMIDAZOLES; MELANOCYTES; MELANOMA; MICE; MICE, INBRED C57BL; NEVUS; PIGMENTATION; PIPERAZINES; PROTO-ONCOGENE PROTEINS; SKIN NEOPLASMS; STAINING AND LABELING; SURVIVAL ANALYSIS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-PROTEIN LIGASES;

MURINAE; MUS;

EID: 78049284499     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/j.1755-148X.2010.00773.x     Document Type: Article

References (73)

1. Abdel-Malek, Z.A., Kadekaro, A.L., and Swope, V.B. (2010). Stepping up melanocytes to the challenge of UV exposure. Pigment Cell Melanoma Res. 23, 171-186.
2. Albino, A.P., Vidal, M.J., Mcnutt, N.S., Shea, C.R., Prieto, V.G., Nanus, D.M., Palmer, J.M., and Hayward, N.K. (1994). Mutation and expression of the p53 gene in human malignant melanoma. Melanoma Res. 4, 35-45.
3. Bae, I., Smith, M.L., Sheikh, M.S., Zhan, Q., Scudiero, D.A., Friend, S.H., O'connor, P.M., and Fornace, A.J., Jr (1996). An abnormality in the p53 pathway following gamma-irradiation in many wild-type p53 human melanoma lines. Cancer Res. 56, 840-847.
4. Bandyopadhyay, D., Gatza, C., Donehower, L.A., and Medrano, E.E. (2005). Analysis of cellular senescence in culture in vivo: the senescence-associated beta-galactosidase assay. Curr. Protoc. Cell Biol. Chapter 18, Unit 18.9.
5. Bardeesy, N., Bastian, B.C., Hezel, A., Pinkel, D., Depinho, R.A., and Chin, L. (2001). Dual inactivation of RB and p53 pathways in RAS-induced melanomas. Mol. Cell. Biol. 21, 2144-2153.
6. Berger, A.J., Camp, R.L., Divito, K.A., Kluger, H.M., Halaban, R., and Rimm, D.L. (2004). Automated quantitative analysis of HDM2 expression in malignant melanoma shows association with early-stage disease and improved outcome. Cancer Res. 64, 8767-8772.
7. Box, N.F., and Terzian, T. (2008). The role of p53 in pigmentation, tanning and melanoma. Pigment Cell Melanoma Res. 21, 525-533.
8. Broome Powell, M., Gause, P.R., Hyman, P., Gregus, J., Lluria-Prevatt, M., Nagle, R., and Bowden, G.T. (1999). Induction of melanoma in TPras transgenic mice. Carcinogenesis 20, 1747-1753.
9. Castresana, J.S., Rubio, M.P., Vazquez, J.J., Idoate, M., Sober, A.J., Seizinger, B.R., and Barnhill, R.L. (1993). Lack of allelic deletion and point mutation as mechanisms of p53 activation in human malignant melanoma. Int. J. Cancer 55, 562-565.
10. Christophorou, M.A., Ringshausen, I., Finch, A.J., Swigart, L.B., and Evan, G.I. (2006). The pathological response to DNA damage does not contribute to p53-mediated tumour suppression. Nature 443, 214-217.
11. Cotter, M.A., Thomas, J., Cassidy, P., Robinette, K., Jenkins, N., Florell, S.R., Leachman, S., Samlowski, W.E., and Grossman, D. (2007). N-acetylcysteine protects melanocytes against oxidative stress/damage and delays onset of ultraviolet-induced melanoma in mice. Clin. Cancer Res. 13, 5952-5958.
12. Cui, R., Widlund, H.R., Feige, E. et al. (2007). Central role of p53 in the suntan response and pathologic hyperpigmentation. Cell 128, 853-864.
13. Dennis, G., Jr, Sherman, B.T., Hosack, D.A., Yang, J., Gao, W., Lane, H.C., and Lempicki, R.A. (2003). DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, P3.
14. Elwood, J.M. (1996). Melanoma and sun exposure. Semin. Oncol. 23, 650-666.
15. Essner, R., Kuo, C.T., Wang, H., Wen, D.R., Turner, R.R., Nguyen, T., and Hoon, D.S. (1998). Prognostic implications of p53 overexpression in cutaneous melanoma from sun-exposed and nonexposed sites. Cancer 82, 309-316.
16. Florenes, V.A., Holm, R., and Fodstad, O. (1995). Accumulation of p53 protein in human malignant melanoma. Relationship to clinical outcome. Melanoma Res. 5, 183-187.
17. Gandini, S., Sera, F., Cattaruzza, M.S., Pasquini, P., Picconi, O., Boyle, P., and Melchi, C.F. (2005). Meta-analysis of risk factors for cutaneous melanoma: II. Sun exposure. Eur. J. Cancer 41, 45-60.
18. Garner, E., and Raj, K. (2008). Protective mechanisms of p53-p21-pRb proteins against DNA damage-induced cell death. Cell Cycle 7, 277-282.
19. Gause, P.R., Lluria-Prevatt, M., Keith, W.N., Balmain, A., Linardopolous, S., Warneke, J., and Powell, M.B. (1997). Chromosomal and genetic alterations of 7, 12-dimethylbenz[a]anthracene-induced melanoma from TP-ras transgenic mice. Mol. Carcinog. 20, 78-87.
20. Goel, V.K., Ibrahim, N., Jiang, G., Singhal, M., Fee, S., Flotte, T., Westmoreland, S., Haluska, F.S., Hinds, P.W., and Haluska, F.G. (2009). Melanocytic nevus-like hyperplasia and melanoma in transgenic BRAFV600E mice. Oncogene 28, 2289-2298.
21. Gorospe, M., Cirielli, C., Wang, X., Seth, P., Capogrossi, M.C., and Holbrook, N.J. (1997). p21(Waf1/Cip1) protects against p53-mediated apoptosis of human melanoma cells. Oncogene 14, 929-935.
22. Goukassian, D.A., Eller, M.S., Yaar, M., and Gilchrest, B.A. (1999). Thymidine dinucleotide mimics the effect of solar simulated irradiation on p53 and p53-regulated proteins. J. Invest. Dermatol. 112, 25-31.
23. Grichnik, J.M. (2006). Kit and melanocyte migration. J. Invest. Dermatol. 126, 945-947.
24. Haass, N.K., and Herlyn, M. (2005). Normal human melanocyte homeostasis as a paradigm for understanding melanoma. J. Investig. Dermatol. Symp. Proc. 10, 153-163.
25. Hacker, E., Muller, H.K., Irwin, N. et al. (2006). Spontaneous and UV radiation-induced multiple metastatic melanomas in Cdk4R24C/R24C/TPras mice. Cancer Res. 66, 2946-2952.
26. Hacker, E., Muller, H.K., Hayward, N., Fahey, P., and Walker, G. (2010). Enhancement of DNA repair using topical T4 endonuclease V does not inhibit melanoma formation in Cdk4(R24C/R24C)/Tyr-Nras(Q61K) mice following neonatal UVR. Pigment Cell Melanoma Res. 23, 121-128.
27. Halaban, R., Cheng, E., Svedine, S., Aron, R., and Hebert, D.N. (2001). Proper folding and endoplasmic reticulum to golgi transport of tyrosinase are induced by its substrates, DOPA and tyrosine. J. Biol. Chem. 276, 11933-11938.
28. Hartmann, A., Blaszyk, H., Cunningham, J.S., Mcgovern, R.M., Schroeder, J.S., Helander, S.D., Pittelkow, M.R., Sommer, S.S., and Kovach, J.S. (1996). Overexpression and mutations of p53 in metastatic malignant melanomas. Int. J. Cancer 67, 313-317.
29. Hay, N. (2005). The Akt-mTOR tango and its relevance to cancer. Cancer Cell 8, 179-183.
30. Henning, J.S., Dusza, S.W., Wang, S.Q., Marghoob, A.A., Rabinovitz, H.S., Polsky, D., and Kopf, A.W. (2007). The CASH (color, architecture, symmetry, and homogeneity) algorithm for dermoscopy. J. Am. Acad. Dermatol. 56, 45-52.
31. Hocker, T., and Tsao, H. (2007). Ultraviolet radiation and melanoma: a systematic review and analysis of reported sequence variants. Hum. Mutat. 28, 578-588.
32. Hong, H., Takahashi, K., Ichisaka, T., Aoi, T., Kanagawa, O., Nakagawa, M., Okita, K., and Yamanaka, S. (2009). Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 460, 1132-1135.
33. Huang, W., Sherman, B.T., and Lempicki, R.A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
34. Hussein, M.R. (2004). The TP53 tumor suppressor gene and melanoma tumorigenesis: is there a relationship? Tumour Biol. 25, 200-207.
35. Karst, A.M., Dai, D.L., Martinka, M., and Li, G. (2005). PUMA expression is significantly reduced in human cutaneous melanomas. Oncogene 24, 1111-1116.
36. Khlgatian, M.K., Hadshiew, I.M., Asawanonda, P., Yaar, M., Eller, M.S., Fujita, M., Norris, D.A., and Gilchrest, B.A. (2002). Tyrosinase gene expression is regulated by p53. J. Invest. Dermatol. 118, 126-132.
37. Lin, T., Chao, C., Saito, S., Mazur, S.J., Murphy, M.E., Appella, E., and Xu, Y. (2005). p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat. Cell Biol. 7, 165-171.
38. Liu, G., Terzian, T., Xiong, S., Van Pelt, C.S., Audiffred, A., Box, N.F., and Lozano, G. (2007). The p53-Mdm2 network in progenitor cell expansion during mouse postnatal development. J. Pathol. 213, 360-368.
39. Lubbe, J., Reichel, M., Burg, G., and Kleihues, P. (1994). Absence of p53 gene mutations in cutaneous melanoma. J. Invest. Dermatol. 102, 819-821.
40. Marrot, L., Belaidi, J.P., Jones, C., Perez, P., and Meunier, J.R. (2005). Molecular responses to stress induced in normal human caucasian melanocytes in culture by exposure to simulated solar UV. Photochem. Photobiol. 81, 367-375.
41. McGill, G.G., Horstmann, M., Widlund, H.R. et al. (2002). Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell 109, 707-718.
42. McGregor, J.M., Yu, C.C., Dublin, E.A., Barnes, D.M., Levison, D.A., and Macdonald, D.M. (1993). p53 immunoreactivity in human malignant melanoma and dysplastic naevi. Br. J. Dermatol. 128, 606-611.
43. Meletis, K., Wirta, V., Hede, S.M., Nister, M., Lundeberg, J., and Frisen, J. (2006). p53 suppresses the self-renewal of adult neural stem cells. Development 133, 363-369.
44. Montano, X., Shamsher, M., Whitehead, P., Dawson, K., and Newton, J. (1994). Analysis of p53 in human cutaneous melanoma cell lines. Oncogene 9, 1455-1459.
45. Moriyama, M., Osawa, M., Mak, S.S. et al. (2006). Notch signaling via Hes1 transcription factor maintains survival of melanoblasts and melanocyte stem cells. J. Cell Biol. 173, 333-339.
46. Nylander, K., Bourdon, J.C., Bray, S.E., Gibbs, N.K., Kay, R., Hart, I., and Hall, P.A. (2000). Transcriptional activation of tyrosinase and TRP-1 by p53 links UV irradiation to the protective tanning response. J. Pathol. 190, 39-46.
47. Papp, T., Jafari, M., and Schiffmann, D. (1996). Lack of p53 mutations and loss of heterozygosity in non-cultured human melanocytic lesions. J. Cancer Res. Clin. Oncol. 122, 541-548.
48. Parant, J., Chavez-Reyes, A., Little, N.A., Yan, W., Reinke, V., Jochemsen, A.G., and Lozano, G. (2001). Rescue of embryonic lethality in Mdm4-null mice by loss of Trp53 suggests a nonoverlapping pathway with MDM2 to regulate p53. Nat. Genet. 29, 92-95.
49. Patton, E.E., Widlund, H.R., Kutok, J.L. et al. (2005). BRAF mutations are sufficient to promote nevi formation and cooperate with p53 in the genesis of melanoma. Curr. Biol. 15, 249-254.
50. Perlis, C., and Herlyn, M. (2004). Recent advances in melanoma biology. Oncologist 9, 182-187.
51. Polsky, D., Bastian, B.C., Hazan, C., Melzer, K., Pack, J., Houghton, A., Busam, K., Cordon-Cardo, C., and Osman, I. (2001). HDM2 protein overexpression, but not gene amplification, is related to tumorigenesis of cutaneous melanoma. Cancer Res. 61, 7642-7646.
52. Polsky, D., Melzer, K., Hazan, C. et al. (2002). HDM2 protein overexpression and prognosis in primary malignant melanoma. J. Natl Cancer Inst. 94, 1803-1806.
53. Powell, M.B., Hyman, P., Bell, O.D., Balmain, A., Brown, K., Alberts, D., and Bowden, G.T. (1995). Hyperpigmentation and melanocytic hyperplasia in transgenic mice expressing the human T24 Ha-ras gene regulated by a mouse tyrosinase promoter. Mol. Carcinog. 12, 82-90.
54. Schoppy, D.W., Ruzankina, Y., and Brown, E.J. (2010). Removing all obstacles: a critical role for p53 in promoting tissue renewal. Cell Cycle 9, 1313-1319.
55. Scott, G., Cassidy, L., and Busacco, A. (1997). Fibronectin suppresses apoptosis in normal human melanocytes through an integrin-dependent mechanism. J. Invest. Dermatol. 108, 147-153.
56. Smalley, K.S., Contractor, R., Haass, N.K. et al. (2007). An organometallic protein kinase inhibitor pharmacologically activates p53 and induces apoptosis in human melanoma cells. Cancer Res. 67, 209-217.
57. Smith, M.L., Ford, J.M., Hollander, M.C., Bortnick, R.A., Amundson, S.A., Seo, Y.R., Deng, C.X., Hanawalt, P.C., and Fornace, A.J., Jr (2000). p53-mediated DNA repair responses to UV radiation: studies of mouse cells lacking p53, p21, and/or gadd45 genes. Mol. Cell. Biol. 20, 3705-3714.
58. Soengas, M.S., and Lowe, S.W. (2003). Apoptosis and melanoma chemoresistance. Oncogene 22, 3138-3151.
59. Soengas, M.S., Capodieci, P., Polsky, D. et al. (2001). Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature 409, 207-211.
60. Sotillo, R., Garcia, J.F., Ortega, S., Martin, J., Dubus, P., Barbacid, M., and Malumbres, M. (2001). Invasive melanoma in Cdk4-targeted mice. Proc. Natl. Acad. Sci. U S A 98, 13312-13317.
61. Sparrow, L.E., English, D.R., Heenan, P.J., Dawkins, H.J., and Taran, J. (1995a). Prognostic significance of p53 over-expression in thin melanomas. Melanoma Res. 5, 387-392.
62. Sparrow, L.E., Soong, R., Dawkins, H.J., Iacopetta, B.J., and Heenan, P.J. (1995b). p53 gene mutation and expression in naevi and melanomas. Melanoma Res. 5, 93-100.
63. Terzian, T., Wang, Y., Van Pelt, C.S., Box, N.F., Travis, E.L., and Lozano, G. (2007). Haploinsufficiency of Mdm2 and Mdm4 in tumorigenesis and development. Mol. Cell. Biol. 27, 5479-5485.
64. Torchia, E.C., Chen, Y., Sheng, H., Katayama, H., Fitzpatrick, J., Brinkley, W.R., Caulin, C., Sen, S., and Roop, D.R. (2009). A genetic variant of Aurora kinase A promotes genomic instability leading to highly malignant skin tumors. Cancer Res. 69, 7207-7215.
65. Vassilev, L.T., Vu, B.T., Graves, B. et al. (2004). In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303, 844-848.
66. Volkenandt, M., Schlegel, U., Nanus, D.M., and Albino, A.P. (1991). Mutational analysis of the human p53 gene in malignant melanoma. Pigment Cell Res. 4, 35-40.
67. Wang, N., and Hebert, D.N. (2006). Tyrosinase maturation through the mammalian secretory pathway: bringing color to life. Pigment Cell Res. 19, 3-18.
68. Weatherhead, S.C., Haniffa, M., and Lawrence, C.M. (2007). Melanomas arising from naevi and de novo melanomas - does origin matter? Br. J. Dermatol. 156, 72-76.
69. Weiss, J., Heine, M., Arden, K.C., Korner, B., Pilch, H., Herbst, R.A., and Jung, E.G. (1995). Mutation and expression of TP53 in malignant melanomas. Recent Results Cancer Res. 139, 137-154.
70. Yamaguchi, Y., Coelho, S.G., Zmudzka, B.Z., Takahashi, K., Beer, J.Z., Hearing, V.J., and Miller, S.A. (2008). Cyclobutane pyrimidine dimer formation and p53 production in human skin after repeated UV irradiation. Exp. Dermatol. 17, 916-924.
71. Yoon, H., Liyanarachchi, S., Wright, F.A., Davuluri, R., Lockman, J.C., De La Chapelle, A., and Pellegata, N.S. (2002). Gene expression profiling of isogenic cells with different TP53 gene dosage reveals numerous genes that are affected by TP53 dosage and identifies CSPG2 as a direct target of p53. Proc. Natl. Acad. Sci. U S A 99, 15632-15637.
72. Yu, H., Mcdaid, R., Lee, J. et al. (2009). The role of BRAF mutation and p53 inactivation during transformation of a subpopulation of primary human melanocytes. Am. J. Pathol. 174, 2367-2377.
73. Zhao, Y., Chaiswing, L., Bakthavatchalu, V., Oberley, T.D., and St Clair, D.K. (2006). Ras mutation promotes p53 activation and apoptosis of skin keratinocytes. Carcinogenesis 27, 1692-1698.