Genome-wide promoter methylation analysis identifies epigenetic silencing of MAPK13 in primary cutaneous melanoma

Pigment Cell and Melanoma Research

Volumn 26, Issue 4, 2013, Pages 542-554

  Gao, Linda ^a   Smit, Marjon A ^b   van den Oord, Joost J ^c   Goeman, Jelle J ^a   Verdegaal, Els M E ^a   van der Burg, Sjoerd H ^a   Stas, Marguerite ^c   Beck, Samuel ^d   Gruis, Nelleke A ^a   Tensen, Cornelis P ^a   Willemze, Rein ^a   Peeper, Daniel S ^b   van Doorn, Remco ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d LEIDEN CYTOLOGY AND PATHOLOGY LABORATORY   (Netherlands)

Author keywords

DNA methylation; Epigenetics; MAPK13; Melanoma; P38; Primary cutaneous melanoma

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 13; TRANSCRIPTION FACTOR HOXA9;

ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CLINICAL ARTICLE; CUTANEOUS MELANOMA; DNA METHYLATION; EPIGENETICS; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MELANOCYTIC NEVUS; MELANOMA CELL; METASTATIC MELANOMA; PROMOTER REGION; PROTEIN EXPRESSION; TUMOR SUPPRESSOR GENE;

CELL PROLIFERATION; CPG ISLANDS; DISEASE PROGRESSION; DNA METHYLATION; EPIGENESIS, GENETIC; EPIGENOMICS; FIBROBLASTS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MELANOCYTES; MELANOMA; MITOGEN-ACTIVATED PROTEIN KINASE 13; NEVUS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROMOTER REGIONS, GENETIC; SKIN NEOPLASMS; SULFITES;

EID: 84879713307     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/pcmr.12096     Document Type: Article

References (49)

1. Askari, N., Diskin, R., Avitzour, M., Capone, R., Livnah, O., and Engelberg, D. (2007). Hyperactive variants of p38α induce, whereas hyperactive variants of p38γ suppress, activating protein 1-mediated transcription. J. Biol. Chem. 282, 91-99.
2. 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 Stat. Methodol. 57, 289-300.
3. Berger, M.F., Hodis, E., Heffernan, T.P. et al. (2012). Melanoma genome sequencing reveals frequent PREX2 mutations. Nature 485, 502-506.
4. Bracken, A.P., Dietrich, N., Pasini, D., Hansen, K.H., and Helin, K. (2006). Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 20, 1123-1136.
5. Carmona, F.J., Villanueva, A., Vidal, A. et al. (2012). Epigenetic disruption of cadherin-11 in human cancer metastasis. J. Pathol. 228, 230-240.
6. Cerezo-Guisado, M.I., Reino, P.D., Remy, G.L., Kuma, Y., Arthur, J.S., Gallego-Ortega, D., and Cuenda, A. (2011). Evidence of p38γ and p38δ involvement in cell transformation processes. Carcinogenesis 32, 1093-1099.
7. Conway, K., Edmiston, S.N., Khondker, Z.S. et al. (2011). DNA-methylation profiling distinguishes malignant melanomas from benign nevi. Pigment Cell Melanoma Res. 24, 352-360.
8. De Carvalho, D., Sharma, S., You, J., Su, S.F., Taberlay, P., Kelly, T., Yang, X., Liang, G., and Jones, P. (2012). DNA methylation screening identifies driver epigenetic events of cancer cell survival. Cancer Cell 21, 655-667.
9. Denk, A.E., Bettstetter, M., Wild, P.J., Hoek, K., Bataille, F., Dietmaier, W., and Bosserhoff, A.K. (2007). Loss of maspin expression contributes to a more invasive potential in malignant melanoma. Pigment Cell Res. 20, 112-119.
10. Edgar, R., Domrachev, M., and Lash, A.E. (2002). Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210.
11. van Eijk, E.R., Licht, J., Schrumpf, M. et al. (2011). Rapid KRAS, EGFR, BRAF and PIK3CA mutation analysis of fine needle aspirates from non-small-cell lung cancer using allele-specific qPCR. PLoS ONE 6, e17791.
12. Fackler, M.J., Umbricht, C.B., Williams, D. et al. (2011). Genome-wide methylation analysis identifies genes specific to breast cancer hormone receptor status and risk of recurrence. Cancer Res. 71, 6195-6207.
13. Furuta, J., Umebayashi, Y., Miyamoto, K., Kikuchi, K., Otsuka, F., Sugimura, T., and Ushijima, T. (2004). Promoter methylation profiling of 30 genes in human malignant melanoma. Cancer Sci. 95, 962-968.
14. Garcia-Manero, G., Daniel, J., Smith, T.L., Kornblau, S.M., Lee, M.S., Kantarjian, H.M., and Issa, J.P. (2002). DNA methylation of multiple promoter-associated CPG islands in adult acute lymphocytic leukemia. Clin. Cancer Res. 8, 2217-2224.
15. Goto, Y., Shinjo, K., Kondo, Y. et al. (2009). Epigenetic profiles distinguish malignant pleural mesothelioma from lung adenocarcinoma. Cancer Res. 69, 9073-9082.
16. Hawkes, W.C., and Alkan, Z. (2012). Delayed cell cycle progression in selenoprotein w depleted cells is regulated by a mitogen-activated protein kinase kinase 4 (MKK4)-p38/c-Jun NH2-terminal kinase (JNK)-p53 pathway. J. Biol. Chem. 287, 27371-27379.
17. Higgins, M.E., Claremont, M., Major, J.E., Sander, C., and Lash, A.E. (2007). Cancer genes: a gene selection resource for cancer genome projects. Nucleic Acids Res. 35, D721-D726.
18. Hodis, E., Watson, I., Kryukov, G. et al. (2012). A landscape of driver mutations in melanoma. Cell 150, 251-263.
19. Huang, D.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.
20. Koga, Y., Pelizzola, M., Cheng, E., Krauthammer, M., Sznol, M., Ariyan, S., Narayan, D., Molinaro, A.M., Halaban, R., and Weissman, S.M. (2009). Genome-wide screen of promoter methylation identifies novel markers in melanoma. Genome Res. 19, 1462-1470.
21. Krauthammer, M., Kong, Y., Ha, B.H. et al. (2012). Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat. Genet. 44, 1006-1014.
22. Kwong, J., Hong, L., Liao, R., Deng, Q., Han, J., and Sun, P. (2009). p38α and p38γ mediate oncogenic ras-induced senescence through differential mechanisms. J. Biol. Chem. 284, 11237-11246.
23. Lee, H., Zhang, P., Herrmann, A. et al. (2012). Acetylated STAT3 is crucial for methylation of tumor-suppressor gene promoters and inhibition by resveratrol results in demethylation. Proc. Natl Acad. Sci. USA 109, 7765-7769.
24. Lian, C., Xu, Y., Ceol, C. et al. (2012). Loss of 5-hydroxymethylcytosine is an epigenetic hallmark of melanoma. Cell 150, 1135-1146.
25. Liu, S., Ren, S., Howell, P., Fodstad, O., and Riker, A.I. (2008). Identification of novel epigenetically modified genes in human melanoma via promoter methylation gene profiling. Pigment Cell Melanoma Res. 21, 545-558.
26. 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.
27. Mooi, W.J., and Peeper, D.S. (2006). Oncogene-induced cell senescence-halting on the road to cancer. N. Engl. J. Med. 355, 1037-1046.
28. Morgenstern, J.P., and Land, H. (1990). Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18, 3587-3596.
29. Muthusamy, V., Duraisamy, S., Bradbury, C.M., Hobbs, C., Curley, D.P., Nelson, B., and Bosenberg, M. (2006). Epigenetic silencing of novel tumor suppressors in malignant melanoma. Cancer Res. 66, 11187-11193.
30. Nikolaev, S.I., Rimoldi, D., Iseli, C. et al. (2012). Exome sequencing identifies recurrent somatic MAP2K1 and MAP2K2 mutations in melanoma. Nat. Genet. 44, 133-139.
31. Noushmehr, H., Weisenberger, D.J., Diefes, K. et al. (2010). Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17, 510-522.
32. Rauch, T.A., Zhong, X., Wu, X., Wang, M., Kernstine, K.H., Wang, Z., Riggs, A.D., and Pfeifer, G.P. (2008). High-resolution mapping of DNA hypermethylation and hypomethylation in lung cancer. Proc. Natl Acad. Sci. USA 105, 252-257.
33. Rothhammer, T., and Bosserhoff, A.K. (2007). Epigenetic events in malignant melanoma. Pigment Cell Res. 20, 92-111.
34. Schindler, E.M., Hindes, A., Gribben, E.L. et al. (2009). p38δ mitogen-activated protein kinase is essential for skin tumor development in mice. Cancer Res. 69, 4648-4655.
35. Shah, N., and Sukumar, S. (2010). The hox genes and their roles in oncogenesis. Nat. Rev. Cancer 10, 361-371.
36. Sigalotti, L., Covre, A., Fratta, E., Parisi, G., Colizzi, F., Rizzo, A., Danielli, R., Nicolay, H.J., Coral, S., and Maio, M. (2010). Epigenetics of human cutaneous melanoma: setting the stage for new therapeutic strategies. J. Transl. Med. 8, 56.
37. Smiraglia, D.J., Rush, L.J., Fruhwald, M.C. et al. (2001). Excessive CpG island hypermethylation in cancer cell lines versus primary human malignancies. Hum. Mol. Genet. 10, 1413-1419.
38. Spugnardi, M., Tommasi, S., Dammann, R., Pfeifer, G.P., and Hoon, D.S.B. (2003). Epigenetic inactivation of RAS association domain family protein 1 (RASSF1A) in malignant cutaneous melanoma. Cancer Res. 63, 1639-1643.
39. Stark, M.S., Woods, S.L., Gartside, M.G. et al. (2012). Frequent somatic mutations in MAP3K5 and MAP3K9 in metastatic melanoma identified by exome sequencing. Nat. Genet. 44, 165-169.
40. Sun, P., Yoshizuka, N., New, L. et al. (2007). PRAK is essential for ras-induced senescence and tumor suppression. Cell 128, 295-308.
41. Tellez, C.S., Shen, L., Estecio, M.R., Jelinek, J., Gershenwald, J.E., and Issa, J.P. (2009). CpG island methylation profiling in human melanoma cell lines. Melanoma Res. 19, 146-155.
42. Toyota, M., Kopecky, K.J., Toyota, M.O., Jair, K.W., Willman, C.L., and Issa, J.P. (2001). Methylation profiling in acute myeloid leukemia. Blood 97, 2823-2829.
43. Vandesompele, J., de Preter, P.K., Pattyn, F., Poppe, B., van Roy, R.N., de Paepe, P.A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034.
44. Vire, E., Brenner, C., Deplus, R. et al. (2006). The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439, 871-874.
45. Vredeveld, L.C.W., Possik, P.A., Smit, M.A. et al. (2012). Abrogation of BRAFV600E-induced senescence by PI3K pathway activation contributes to melanomagenesis. Genes Dev. 26, 1055-1069.
46. Wagner, E.F., and Nebreda, A.R. (2009). Signal integration by JNK and p38 MAPK pathways in cancer development. Nat. Rev. Cancer 9, 537-549.
47. Widschwendter, M., Fiegl, H., Egle, D. et al. (2007). Epigenetic stem cell signature in cancer. Nat. Genet. 39, 157-158.
48. van Wieringen, W.N., van de Wiel, M.A., and van der Vaart, A.W. (2008). A test for partial differential expression. J. Am. Stat. Assoc. 103, 1039-1049.
49. 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.