A prognostic signature of defective p53-dependent G1 checkpoint function in melanoma cell lines

Pigment Cell and Melanoma Research

Volumn 25, Issue 4, 2012, Pages 514-526

  Carson, Craig ^a   Omolo, Bernard ^b   Chu, Haitao ^c   Zhou, Yingchun ^d   Sambade, Maria J ^d   Peters, Eldon C ^d   Tompkins, Patrick ^d   Simpson, Dennis A ^a,d   Thomas, Nancy E ^a,d   Fan, Cheng ^d   Sarasin, Alain ^e   Dessen, Philippe ^e   Shields, Janiel M ^a   Ibrahim, Joseph G ^d,f   Kaufmann, William K ^a,d  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTH CAROLINA UPSTATE   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

^e INSTITUT GUSTAVE ROUSSY   (France)

^f The University of North Carolina at Chapel Hill   (United States)

Author keywords

Checkpoint; Expression; Function; Gene; Melanoma; P53; Signature

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 2A; PEPTIDES AND PROTEINS; PROTEIN DDB2; PROTEIN P53; PROTEIN RRM2B; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CANCER PROGNOSIS; DISTANT METASTASIS FREE SURVIVAL; G1 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; HUMAN; HUMAN CELL; MELANOCYTE; MELANOMA CELL; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; RADIOSENSITIVITY;

CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA PROBES; G1 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELANOCYTES; MELANOMA; PROGNOSIS; SKIN NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84862676997     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/j.1755-148X.2012.01010.x     Document Type: Article

References (74)

1. Abbas, T., and Dutta, A. (2009). p21 in cancer: intricate networks and multiple activities. Nat. Rev. Cancer 9, 400-414.
2. Abukhdeir, A.M., and Park, B.H. (2008). P21 and p27: roles in carcinogenesis and drug resistance. Expert Rev. Mol. Med. 10, e19.
3. Alonso, S.R., Ortiz, P., Pollan, M. et al. (2004). Progression in cutaneous malignant melanoma is associated with distinct expression profiles: a tissue microarray-based study. Am. J. Pathol. 164, 193-203.
4. Amundson, S.A., Do, K.T., Vinikoor, L.C. et al. (2008). Integrating global gene expression and radiation survival parameters across the 60 cell lines of the National Cancer Institute Anticancer Drug Screen. Cancer Res. 68, 415-424.
5. Bandyopadhyay, D., Curry, J.L., Lin, Q., Richards, H.W., Chen, D., Hornsby, P.J., Timchenko, N.A., and Medrano, E.E. (2007). Dynamic assembly of chromatin complexes during cellular senescence: implications for the growth arrest of human melanocytic nevi. Aging Cell 6, 577-591.
6. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B (Methodol.) 57, 289-300.
7. Berns, K., Hijmans, E.M., Mullenders, J. et al. (2004). A large-scale RNAi screen in human cells identifies new components of the p53 pathway. Nature 428, 431-437.
8. Bild, A.H., Parker, J.S., Gustafson, A.M. et al. (2009). An integration of complementary strategies for gene-expression analysis to reveal novel therapeutic opportunities for breast cancer. Breast Cancer Res. 11, R55.
9. Blokx, W.A., Van Dijk, M.C., and Ruiter, D.J. (2010). Molecular cytogenetics of cutaneous melanocytic lesions - diagnostic, prognostic and therapeutic aspects. Histopathology 56, 121-132.
10. Carr, J., and Mackie, R.M. (1994). Point mutations in the N-ras oncogene in malignant melanoma and congenital naevi. Br. J. Dermatol. 131, 72-77.
11. Chen, B., Simpson, D.A., Zhou, Y., Mitra, A., Mitchell, D.L., Cordeiro-Stone, M., and Kaufmann, W.K. (2009). Human papilloma virus type16 E6 deregulates CHK1 and sensitizes human fibroblasts to environmental carcinogens independently of its effect on p53. Cell Cycle 8, 1775-1787.
12. Cheung, M., Sharma, A., Madhunapantula, S.V., and Robertson, G.P. (2008). Akt3 and mutant V600E B-Raf cooperate to promote early melanoma development. Cancer Res. 68, 3429-3439.
13. Chudnovsky, Y., Adams, A.E., Robbins, P.B., Lin, Q., and Khavari, P.A. (2005). Use of human tissue to assess the oncogenic activity of melanoma-associated mutations. Nat. Genet. 37, 745-749.
14. Daniotti, M., Oggionni, M., Ranzani, T. et al. (2004). BRAF alterations are associated with complex mutational profiles in malignant melanoma. Oncogene 23, 5968-5977.
15. Degenhardt, Y., Greshock, J., Laquerre, S. et al. (2010). Sensitivity of cancer cells to Plk1 inhibitor GSK461364A is associated with loss of p53 function and chromosome instability. Mol. Cancer Ther. 9, 2079-2089.
16. Deisenroth, C., and Zhang, Y. (2010). Ribosome biogenesis surveillance: probing the ribosomal protein-Mdm2-p53 pathway. Oncogene 29, 4253-4260.
17. Dornan, D., Wertz, I., Shimizu, H., Arnott, D., Frantz, G.D., Dowd, P., O'rourke, K., Koeppen, H., and Dixit, V.M. (2004). The ubiquitin ligase COP1 is a critical negative regulator of p53. Nature 429, 86-92.
18. Dulic, V., Kaufmann, W.K., Wilson, S.J., Tlsty, T.D., Lees, E., Harper, J.W., Elledge, S.J., and Reed, S.I. (1994). p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76, 1013-1023.
19. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc. Natl Acad. Sci. U S A 95, 14863-14868.
20. Garraway, L.A., Widlund, H.R., Rubin, M.A. et al. (2005). Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436, 117-122.
21. Gould Rothberg, B.E., Berger, A.J., Molinaro, A.M., Subtil, A., Krauthammer, M.O., Camp, R.L., Bradley, W.R., Ariyan, S., Kluger, H.M., and Rimm, D.L. (2009). Melanoma prognostic model using tissue microarrays and genetic algorithms. J. Clin. Oncol. 27, 5772-5780.
22. Gray-Schopfer, V.C., Cheong, S.C., Chong, H., Chow, J., Moss, T., Abdel-Malek, Z.A., Marais, R., Wynford-Thomas, D., and Bennett, D.C. (2006). Cellular senescence in naevi and immortalisation in melanoma: a role for p16? Br. J. Cancer 95, 496-505.
23. Haferkamp, S., Scurr, L.L., Becker, T.M., Frausto, M., Kefford, R.F., and Rizos, H. (2009a). Oncogene-induced senescence does not require the p16(INK4a) or p14ARF melanoma tumor suppressors. J. Invest. Dermatol. 129, 1983-1991.
24. Haferkamp, S., Tran, S.L., Becker, T.M., Scurr, L.L., Kefford, R.F., and Rizos, H. (2009b). The relative contributions of the p53 and pRb pathways in oncogene-induced melanocyte senescence. Aging (Albany NY) 1, 542-556.
25. Hanahan, D., and Weinberg, R.A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
26. Hoek, K.S., and Goding, C.R. (2010). Cancer stem cells versus phenotype-switching in melanoma. Pigment Cell Melanoma Res. 23, 746-759.
27. Hoek, K.S., Schlegel, N.C., Brafford, P. et al. (2006). Metastatic potential of melanomas defined by specific gene expression profiles with no BRAF signature. Pigment Cell Res. 19, 290-302.
28. Huarte, M., Guttman, M., Feldser, D. et al. (2010). A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142, 409-419.
29. Ivanov, G.S., Ivanova, T., Kurash, J., Ivanov, A., Chuikov, S., Gizatullin, F., Herrera-Medina, E.M., Rauscher, 3rd, F., Reinberg, D., and Barlev, N.A. (2007). Methylation-acetylation interplay activates p53 in response to DNA damage. Mol. Cell. Biol. 27, 6756-6769.
30. Ji, Z., Njauw, C.N., Taylor, M., Neel, V., Flaherty, K.T., and Tsao, H. (2012). p53 rescue through HDM2 antagonism suppresses melanoma growth and potentiates MEK inhibition. J. Invest. Dermatol. 132, 356-364.
31. Kastan, M.B., Onyekwere, O., Sidransky, D., Volgelstein, B., and Craig, R. (1991). Participation of p53 protein in the cellular responses to DNA damage. Cancer Res. 51, 6304-6311.
32. Kastan, M.B., Zhan, Q., El-Deiry, W.S., Carrier, F., Jacks, T., Walsh, W.V., Plunkett, B.S., Vogelstein, B., and Fornace Jr, A.J. (1992). A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell 71, 587-597.
33. Kaufmann, W.K., and Kaufman, D.G. (1993). Cell cycle control, DNA repair and initiation of carcinogenesis. FASEB J. 7, 1188-1191.
34. Kaufmann, W.K., Nevis, K.R., Qu, P. et al. (2008). Defective cell cycle checkpoint functions in melanoma are associated with altered patterns of gene expression. J. Invest. Dermatol. 128, 175-187.
35. Lane, D., and Levine, A. (2010). p53 Research: the past thirty years and the next thirty years. Cold Spring Harb. Perspect. Biol. 2, a000893.
36. Leikam, C., Hufnagel, A., Schartl, M., and Meierjohann, S. (2008). Oncogene activation in melanocytes links reactive oxygen to multinucleated phenotype and senescence. Oncogene 27, 7070-7082.
37. Levine, A.J. (2011). Introduction: the changing directions of p53 research. Genes Cancer 2, 382-384.
38. Lin, W.M., Baker, A.C., Beroukhim, R. et al. (2008). Modeling genomic diversity and tumor dependency in malignant melanoma. Cancer Res. 68, 664-673.
39. Lu, X., Nguyen, T.A., Zhang, X., and Donehower, L.A. (2008). The Wip1 phosphatase and Mdm2: cracking the "Wip" on p53 stability. Cell Cycle 7, 164-168.
40. Ma, C.X., Janetka, J.W., and Piwnica-Worms, H. (2011). Death by releasing the breaks: CHK1 inhibitors as cancer therapeutics. Trends Mol. Med. 17, 88-96.
41. Meek, D.W., and Anderson, C.W. (2009). Posttranslational Modification of p53: cooperative integrators of function. Cold Spring Harb. Perspect. Biol. 1, a000950.
42. Michaloglou, C., Vredeveld, L.C., Soengas, M.S., Denoyelle, C., Kuilman, T., Van Der Horst, C.M., Majoor, D.M., Shay, J.W., Mooi, W.J., and Peeper, D.S. (2005). BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 436, 720-724.
43. Miracco, C., Pacenti, L., Santopietro, R., Laurini, L., Biagioli, M., and Luzi, P. (2000). Evaluation of telomerase activity in cutaneous melanocytic proliferations. Hum. Pathol. 31, 1018-1021.
44. Muller, P.A., Vousden, K.H., and Norman, J.C. (2011). p53 and its mutants in tumor cell migration and invasion. J. Cell Biol. 192, 209-218.
45. Murakami, I., Hiyama, K., Ishioka, S., Yamakido, M., Kasagi, F., and Yokosaki, Y. (2000). p53 gene mutations are associated with shortened survival in patients with advanced non-small cell lung cancer: an analysis of medically managed patients. Clin. Cancer Res. 6, 526-530.
46. Negrini, S., Gorgoulis, V.G., and Halazonetis, T.D. (2010). Genomic instability - an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol. 11, 220-228.
47. Ofir-Rosenfeld, Y., Boggs, K., Michael, D., Kastan, M.B., and Oren, M. (2008). Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26. Mol. Cell 32, 180-189.
48. Papp, T., Pemsel, H., Zimmermann, R., Bastrop, R., Weiss, D.G., and Schiffmann, D. (1999). Mutational analysis of the N-ras, p53, p16INK4a, CDK4, and MC1R genes in human congenital melanocytic naevi. J. Med. Genet. 36, 610-614.
49. Poon, R.Y., and Hunter, T. (1998). Expression of a novel form of p21Cip1/Waf1 in UV-irradiated and transformed cells. Oncogene 16, 1333-1343.
50. Poyraz, A., Akyurek, N., Gonul, Ii., and Erdem, O. (2004). P21 and Bax expression in cutaneous malignant melanomas: correlation with histologic prognostic parameters. J. Exp. Clin. Cancer Res. 23, 625-631.
51. Sambade, M.J., Peters, E.C., Thomas, N.E., Kaufmann, W.K., Kimple, R.J., and Shields, J.M. (2011). Melanoma cells show a heterogeneous range of sensitivity to ionizing radiation and are radiosensitized by inhibition of B-RAF with PLX-4032. Radiother. Oncol. 98, 394-399.
52. Satyamoorthy, K., Chehab, N.H., Waterman, M.J., Lien, M.C., El-Deiry, W.S., Herlyn, M., and Halazonetis, T.D. (2000). Aberrant regulation and function of wild-type p53 in radioresistant melanoma cells. Cell Growth Differ. 11, 467-474.
53. Schwartz, J.L., Jordan, R., Kaufmann, W.K., Rasey, J., Russell, K.J., and Weichselbaum, R.R. (2000). Evidence for the expression of radiation-induced potentially lethal damage being a p53-dependent process. Int. J. Radiat. Biol. 76, 1037-1043.
54. Shao, R.G., Cao, C.X., Shimizu, T., O'connor, P.M., Kohn, K.W., and Pommier, Y. (1997). Abrogation of an S-phase checkpoint and potentiation of camptothecin cytotoxicity by 7-hydroxystaurosporine (UCN-01) in human cancer cell lines, possibly influenced by p53 function. Cancer Res. 57, 4029-4035.
55. Shields, J.M., Thomas, N.E., Cregger, M. et al. (2007). Lack of extracellular signal-regulated kinase mitogen-activated protein kinase signaling shows a new type of melanoma. Cancer Res. 67, 1502-1512.
56. Simon, R., Lam, A., Li, M.C., Ngan, M., Menenzes, S., and Zhao, Y. (2007). Analysis of gene expression data using BRB-array tools. Cancer Inform. 3, 11-17.
57. Simpson, D.A., Livanos, E., Heffernan, T.P., and Kaufmann, W.K. (2005). Telomerase expression is sufficient for chromosomal integrity in cells lacking p53 dependent G1 checkpoint function. J. Carcinog. 4, 18.
58. Sloan, A.E., Nock, C.J., and Einstein, D.B. (2009). Diagnosis and treatment of melanoma brain metastasis: a literature review. Cancer Control 16, 248-255.
59. Soo, J.K., Mackenzie Ross, A.D., Kallenberg, D.M. et al. (2011). Malignancy without immortality? Cellular immortalization as a possible late event in melanoma progression. Pigment Cell Melanoma Res. 24, 490-503.
60. Stark, M., and Hayward, N. (2007). Genome-wide loss of heterozygosity and copy number analysis in melanoma using high-density single-nucleotide polymorphism arrays. Cancer Res. 67, 2632-2642.
61. Stretch, J.R., Gatter, K.C., Ralfkiaer, E., Lane, D.P., and Harris, A.L. (1991). Expression of mutant p53 in melanoma. Cancer Res. 51, 5976-5979.
62. Terzian, T., Torchia, E.C., Dai, D. et al. (2010). p53 prevents progression of nevi to melanoma predominantly through cell cycle regulation. Pigment Cell Melanoma Res. 23, 781-794.
63. Wajapeyee, N., Serra, R.W., Zhu, X., Mahalingam, M., and Green, M.R. (2008). Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 132, 363-374.
64. Walker, G.J., Flores, J.F., Glendening, J.M., Lin, A.H., Markl, I.D., and Fountain, J.W. (1998). Virtually 100% of melanoma cell lines harbor alterations at the DNA level within CDKN2A, CDKN2B, or one of their downstream targets. Genes Chromosom. Cancer 22, 157-163.
65. Wang, L., He, G., Zhang, P., Wang, X., Jiang, M., and Yu, L. (2010). Interplay between MDM2, MDMX, Pirh2 and COP1: the negative regulators of p53. Mol. Biol. Rep. 38, 229-236.
66. Weiss, J., Schwechheimer, K., Cavenee, W.K., Herlyn, M., and Arden, K.C. (1993). Mutation and expression of the p53 gene in malignant melanoma cell lines. Int. J. Cancer 54, 693-699.
67. Winnepenninckx, V., Lazar, V., Michiels, S. et al. (2006). Gene expression profiling of primary cutaneous melanoma and clinical outcome. J. Natl Cancer Inst. 98, 472-482.
68. Witten, D.M., and Tibshirani, R. (2009). Covariance-regularized regression and classification for high-dimensional problems. J. R. Stat. Soc. Series B Stat. Methodol. 71, 615-636.
69. Yadavilli, S., Mayo, L.D., Higgins, M., Lain, S., Hegde, V., and Deutsch, W.A. (2009). Ribosomal protein S3: a multi-functional protein that interacts with both p53 and MDM2 through its KH domain. DNA Repair (Amst.) 8, 1215-1224.
70. 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.
71. Zhang, X., Lin, L., Guo, H., Yang, J., Jones, S.N., Jochemsen, A., and Lu, X. (2009). Phosphorylation and degradation of MdmX is inhibited by Wip1 phosphatase in the DNA damage response. Cancer Res. 69, 7960-7968.
72. Zhao, Y., and Simon, R. (2010). Development and validation of predictive indices for a continuous outcome using gene expression profiles. Cancer Inform. 9, 105-114.
73. Zhou, T., Chou, J., Zhou, Y., Simpson, D.A., Cao, F., Bushel, P.R., Paules, R.S., and Kaufmann, W.K. (2007). Ataxia telangiectasia-mutated dependent DNA damage checkpoint functions regulate gene expression in human fibroblasts. Mol. Cancer Res. 5, 813-822.
74. Zhuang, D., Mannava, S., Grachtchouk, V. et al. (2008). C-MYC overexpression is required for continuous suppression of oncogene-induced senescence in melanoma cells. Oncogene 27, 6623-6634.