Epigenome-wide DNA methylation landscape of melanoma progression to brain metastasis reveals aberrations on homeobox d cluster associated with prognosis

Human Molecular Genetics

Volumn 23, Issue 1, 2014, Pages 226-238

  Marzese, Diego M ^a   Scolyer, Richard A ^c,d,e   Huynh, Jamie L ^a   Huang, Sharon K ^a   Hirose, Hajime ^a   Chong, Kelly K ^a   Kiyohara, Eiji ^a   Wang, Jinhua ^a   Kawas, Neal P ^a   Donovan, Nicholas C ^a   Hata, Keisuke ^a   Wilmott, James S ^e   Murali, Rajmohan ^f,g   Buckland, Michael E ^d   Shivalingam, Brindha ^e   Thompson, John F ^d,e   Morton, Donald L ^a   Kelly, Daniel F ^a,b   Hoon, Dave S B ^a  

^a JOHN WAYNE CANCER INSTITUTE   (United States)

^b SAINT JOHN'S HEALTH CENTER   (United States)

^c ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e MELANOMA INSTITUTE AUSTRALIA   (Australia)

^f Department of Pathology ^*  (United States)

^g MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BUB3 PROTEIN; HISTONE H2A; HISTONE H2B; HOMEODOMAIN PROTEIN; HOX PROTEIN; INSULIN RECEPTOR SUBSTRATE 2; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN HOXD9; PROTEIN KINASE B; RAC2 PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN;

ARTICLE; BRAIN METASTASIS; CANCER PROGNOSIS; CANCER STAGING; CHROMATIN; COHORT ANALYSIS; CONTROLLED STUDY; COPY NUMBER VARIATION; CPG ISLAND; CUTANEOUS MELANOMA; DEMETHYLATION; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENETIC ASSOCIATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MELANOMA BRAIN METASTASIS; MELANOMA CELL; MELANOMA METASTASIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR CELL LINE; TUMOR GROWTH;

BRAIN NEOPLASMS; CELL LINE, TUMOR; COHORT STUDIES; CPG ISLANDS; DISEASE PROGRESSION; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENES, HOMEOBOX; GENOME, HUMAN; HOMEODOMAIN PROTEINS; HUMANS; LYMPHATIC METASTASIS; MELANOMA; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROGNOSIS; PROMOTER REGIONS, GENETIC; SURVIVAL RATE; TREATMENT OUTCOME;

EID: 84887365803     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt420     Document Type: Article

References (60)

1. Siegel, R., Naishadham, D. and Jemal, A. (2013) Cancer statistics, 2013. CA Cancer J. Clin., 63, 11-30.
2. Miller, A.J. and Mihm, M.C. Jr (2006) Melanoma. N. Engl. J. Med., 355, 51-65.
3. Denkins, Y., Reiland, J., Roy, M., Sinnappah-Kang, N.D., Galjour, J., Murry, B.P., Blust, J., Aucoin, R. and Marchetti, D. (2004) Brain metastases in melanoma: roles of neurotrophins. Neuro. Oncol., 6, 154-165.
4. Lonser, R.R., Song, D.K., Klapper, J., Hagan, M., Auh, S., Kerr, P.B., Citrin, D.E., Heiss, J.D., Camphausen, K. and Rosenberg, S.A. (2011) Surgical management of melanoma brain metastases in patients treated with immunotherapy. J. Neurosurg., 115, 30-36.
5. Valastyan, S. and Weinberg, R.A. (2011) Tumor metastasis: molecular insights and evolving paradigms. Cell, 147, 275-292.
6. Sandoval, J., Heyn, H., Moran, S., Serra-Musach, J., Pujana, M.A., Bibikova, M. and Esteller, M. (2011) Validation of a DNA methylation microarray for 450 000 CpG sites in the human genome. Epigenetics, 6, 692-702.
7. Jones, P.A. and Baylin, S.B. (2007) The epigenomics of cancer. Cell, 128, 683-692.
8. Esteller, M.(2008) Epigenetics in cancer. N. Engl. J. Med., 358, 1148-1159.
9. Jones, P.A. (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Gene.t, 13, 484-492.
10. Varley, K.E., Gertz, J., Bowling, K.M., Parker, S.L., Reddy, T.E., Pauli-Behn, F., Cross, M.K., Williams, B.A., Stamatoyannopoulos, J.A., Crawford, G.E. et al. (2013) Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res., 23, 555-567.
11. Irizarry, R.A., Ladd-Acosta, C., Wen, B., Wu, Z., Montano, C., Onyango, P., Cui, H., Gabo, K., Rongione, M., Webster, M. et al. (2009) The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet., 41, 178-186.
12. Bibikova, M., Barnes, B., Tsan, C., Ho, V., Klotzle, B., Le, J.M., Delano, D., Zhang, L., Schroth, G.P., Gunderson, K.L. et al. (2011) High density DNA methylation array with single CpG site resolution. Genomics, 98, 288-295.
13. Mori, T., Martinez, S.R., O'Day, S.J., Morton, D.L., Umetani, N., Kitago, M., Tanemura, A., Nguyen, S.L., Tran, A.N., Wang, H.J. et al. (2006) Estrogen receptor-alpha methylation predicts melanoma progression. Cancer Res., 66, 6692-6698.
14. Tanemura, A., Terando, A.M., Sim, M.S., van Hoesel, A.Q., de Maat, M.F., Morton, D.L. and Hoon, D.S. (2009) CpG island methylator phenotype predicts progression of malignant melanoma. Clin. Cancer Res., 15, 1801-1807.
15. Hoon, D.S., Ferris, R., Tanaka, R., Chong, K.K., Alix-Panabieres, C. and Pantel, K. (2011) Molecular mechanisms of metastasis. J. Surg. Oncol., 103, 508-517.
16. Koyanagi, K., Mori, T., O'Day, S.J., Martinez, S.R., Wang, H.J. and Hoon, D.S. (2006) Association of circulating tumor cells with serum tumor-related methylatedDNAin peripheral blood of melanoma patients. Cancer Res., 66, 6111-6117.
17. Hoshimoto, S., Kuo, C.T., Chong, K.K., Takeshima, T.L., Takei, Y., Li, M.W., Huang, S.K., Sim, M.S., Morton, D.L. and Hoon, D.S. (2012) AIM1 and LINE-1 epigenetic aberrations in tumor and serum relate to melanoma progression and disease outcome. J. Invest. Dermatol., 132, 1689-1697.
18. 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.
19. Sigalotti, L., Covre, A., Fratta, E., Parisi, G., Sonego, P., Colizzi, F., Coral, S., Massarut, S., Kirkwood, J.M. and Maio, M. (2012) Whole genome methylation profiles as independent markers of survival in stage iiic melanoma patients. J. Transl. Med., 10, 185.
20. Lister, R., Pelizzola, M., Dowen, R.H., Hawkins, R.D., Hon, G., Tonti-Filippini, J., Nery, J.R., Lee, L., Ye, Z., Ngo, Q.M. et al. (2009)Human DNA methylomes at base resolution show widespread epigenomic differences. Nature, 462, 315-322.
21. Schroeder, D.I., Lott, P., Korf, I. and LaSalle, J.M. (2011) Large-scale methylation domains mark a functional subset of neuronally expressed genes. Genome Res., 21, 1583-1591.
22. Cao, L., Li, W., Kim, S., Brodie, S.G. and Deng, C.X. (2003) Senescence, aging, and malignant transformation mediated by p53 in mice lacking the Brca1 full-length isoform. Genes. Dev., 17, 201-213.
23. Baker, D.J., Jeganathan, K.B., Malureanu, L., Perez-Terzic, C., Terzic, A. and van Deursen, J.M. (2006) Early aging-associated phenotypes in Bub3/ Rae1 haploinsufficient mice. J. Cell Biol., 172, 529-540.
24. Maeda, K., Hamada, J., Takahashi, Y., Tada, M., Yamamoto, Y., Sugihara, T. and Moriuchi, T. (2005) Altered expressions of HOX genes in human cutaneous malignant melanoma. Int. J. Cancer, 114, 436-441.
25. Song, L., Zhang, Z., Grasfeder, L.L., Boyle, A.P., Giresi, P.G., Lee, B.K., Sheffield, N.C., Graf, S., Huss, M., Keefe, D. et al. (2011) Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res., 21, 1757-1767.
26. Pandiyan, K., You, J.S., Yang, X., Dai, C., Zhou, X.J., Baylin, S.B., Jones, P.A. and Liang, G. (2013) Functional DNA demethylation is accompanied by chromatin accessibility. Nucleic Acids Res., 41, 3973-3985.
27. The ENCODE Project Consortium. (2011) A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol., 9, e1001046.
28. Bernstein, B.E., Stamatoyannopoulos, J.A., Costello, J.F., Ren, B., Milosavljevic, A., Meissner, A., Kellis, M., Marra, M.A., Beaudet, A.L., Ecker, J.R. et al. (2010) The NIH roadmap epigenomics mapping consortium. Nat. Biotechnol., 28, 1045-1048.
29. Mihic-Probst, D., Ikenberg, K., Tinguely, M., Schraml, P., Behnke, S., Seifert, B., Civenni, G., Sommer, L., Moch, H. and Dummer, R. (2012) Tumor cell plasticity and angiogenesis in human melanomas. PLoS One, 7, e33571.
30. Pujadas, E. and Feinberg, A.P. (2012) Regulated noise in the epigenetic landscape of development and disease. Cell, 148, 1123-1131.
31. Wu, C.Y., Tsai, Y.P., Wu, M.Z., Teng, S.C. and Wu, K.J. (2012) Epigenetic reprogramming and post-transcriptional regulation during the epithelial- mesenchymal transition. Trends Genet., 28, 454-463.
32. Martinez, R. and Esteller, M. (2010) The DNA methylome of glioblastoma multiforme. Neurobiol. Dis., 39, 40-46.
33. Torano, E.G., Petrus, S., Fernandez, A.F. and Fraga, M.F. (2012) Global DNA hypomethylation in cancer: review of validated methods and clinical significance. Clin. Chem. Lab. Med., 50, 1733-1742.
34. Hon, G.C., Hawkins, R.D., Caballero, O.L., Lo, C., Lister, R., Pelizzola, M., Valsesia, A., Ye, Z., Kuan, S., Edsall, L.E. et al. (2012) Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer. Genome Res., 22, 246-258.
35. Schroeder, D.I., Blair, J.D., Lott, P., Yu, H.O., Hong, D., Crary, F., Ashwood, P., Walker, C., Korf, I., Robinson, W.P. et al. (2013) The human placenta methylome. Proc. Natl. Acad. Sci. U S A, 110, 6037-6042.
36. Lister, R. and Ecker, J.R. (2009) Finding the fifth base: genome-wide sequencing of cytosine methylation. Genome Res., 19, 959-966.
37. Gutierrez-Arcelus, M., Lappalainen, T., Montgomery, S.B., Buil, A., Ongen, H., Yurovsky, A., Bryois, J., Giger, T., Romano, L., Planchon, A. et al. (2013) Passive and active DNA methylation and the interplay with genetic variation in gene regulation. Elife, 2, e00523.
38. Deaton, A.M., Webb, S., Kerr, A.R., Illingworth, R.S., Guy, J., Andrews, R. and Bird, A. (2011) Cell type-specific DNA methylation at intragenic CpG islands in the immune system. Genome Res., 21, 1074-1086.
39. Orom, U.A., Derrien, T., Beringer, M., Gumireddy, K., Gardini, A., Bussotti, G., Lai, F., Zytnicki, M., Notredame, C., Huang, Q. et al. (2010) Long noncodingRNAswith enhancer-like function in human cells. Cell, 143, 46- 58.
40. Hanahan, D. and Weinberg, R.A. (2011) Hallmarks of cancer: the next generation. Cell, 144, 646-674.
41. Marty, T., Vigano, M.A., Ribeiro, C., Nussbaumer, U., Grieder, N.C. and Affolter, M. (2001) A HOX complex, a repressor element and a 50 bp sequence confer regional specificity to a DPP-responsive enhancer. Development, 128, 2833-2845.
42. Tabuse, M., Ohta, S., Ohashi, Y., Fukaya, R., Misawa, A., Yoshida, K., Kawase, T., Saya, H., Thirant, C., Chneiweiss, H. et al. (2011) Functional analysis of HOXD9 in human gliomas and glioma cancer stem cells. Mol. Cancer, 10, 60.
43. Gao, L., Smit, M.A., van den Oord, J.J., Goeman, J.J., Verdegaal, E.M., van der Burg, S.H., Stas, M., Beck, S., Gruis, N.A., Tensen, C.P. et al. (2013) Genome-wide promoter methylation analysis identifies epigenetic silencing ofMAPK13in primary cutaneous melanoma. Pigment Cell Melanoma Res., 26, 542-554.
44. Wardwell-Ozgo, J., Dogruluk, T., Gifford, A., Zhang, Y., Heffernan, T.P., van Doorn, R., Creighton, C.J., Chin, L. and Scott, K.L. (2013) HOXA1 drives melanoma tumor growth and metastasis and elicits an invasion gene expression signature that prognosticates clinical outcome. Oncogene. doi:10.1038/onc.2013.30.
45. Cantile, M., Scognamiglio, G., Anniciello, A., Farina, M., Gentilcore, G., Santonastaso, C., Fulciniti, F., Cillo, C., Franco, R., Ascierto, P.A. et al. (2012) IncreasedHOXC13 expression in metastatic melanoma progression. J. Transl. Med., 10, 91.
46. Braig, S., Mueller, D.W., Rothhammer, T. and Bosserhoff, A.K. (2010) MicroRNA miR-196a is a central regulator of HOX-B7 and BMP4 expression in malignant melanoma. Cell Mol. Life Sci., 67, 3535-3548.
47. Tschopp, P. and Duboule, D. (2011)Aregulatory 'landscape effect' over the HoxD cluster. Dev. Biol., 351, 288-296.
48. Simon, J.A. (2010) Chromatin compaction at Hox Loci: a Polycomb tale beyond histone tails. Mol. Cell, 38, 321-322.
49. Isono, K., Mizutani-Koseki, Y., Komori, T., Schmidt-Zachmann, M.S. and Koseki, H. (2005) Mammalian polycomb-mediated repression of Hox genes requires the essential spliceosomal protein Sf3b1. Genes Dev., 19, 536-541.
50. Barth, A., Wanek, L.A. and Morton, D.L. (1995) Prognostic factors in 1,521 melanoma patients with distant metastases. J. Am. Coll. Surg., 181, 193- 201.
51. van Hoesel, A.Q., van de Velde, C.J., Kuppen, P.J., Liefers, G.J., Putter, H., Sato, Y., Elashoff, D.A., Turner, R.R., Shamonki, J.M., de Kruijf, E.M. et al. (2012) Hypomethylation of LINE-1 in primary tumor has poor prognosis in young breast cancer patients: a retrospective cohort study. Breast Cancer Res. Treat., 134, 1103-1114.
52. Hinoue, T., Weisenberger, D.J., Lange, C.P., Shen, H., Byun, H.M.,VanDen Berg, D., Malik, S., Pan, F., Noushmehr, H., van Dijk, C.M. et al. (2011) Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res., 22, 271-282.
53. Sunami, E., de Maat, M., Vu, A., Turner, R.R. and Hoon, D.S. (2011)LINE-1 hypomethylation during primary colon cancer progression. PLoS One, 6, e18884.
54. Umetani, N., de Maat, M.F., Mori, T., Takeuchi, H. and Hoon, D.S. (2005) Synthesis of universal unmethylated control DNA by nested whole genome amplification with phi29 DNA polymerase. Biochem. Biophys. Res. Commun., 329, 219-223.
55. Shinojima, T., Yu, Q., Huang, S.K., Li, M., Mizuno, R., Liu, E.T., Hoon, D.S. and Lessard, L. (2012) Heterogeneous epigenetic regulation of TIMP3 in prostate cancer. Epigenetics., 7, 1279-1289.
56. Saeed, A.I., Bhagabati, N.K., Braisted, J.C., Liang, W., Sharov, V., Howe, E.A., Li, J., Thiagarajan, M., White, J.A. and Quackenbush, J. (2006) TM4 microarray software suite. Methods Enzymol., 411, 134-193.
57. Benson, G. (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res., 27, 573-580.
58. Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O., Blondel, M., Prettenhofer, P., Weiss, R., Dubourg, V. et al. (2011) Scikit-learn: Machine Learning in Python. J. Mach. Learn. Res., 12, 2825- 2830.
59. Hansen, K.D., Timp, W., Bravo, H.C., Sabunciyan, S., Langmead, B., McDonald, O.G., Wen, B., Wu, H., Liu, Y., Diep, D. et al. (2012) Increased methylation variation in epigenetic domains across cancer types. Nat. Genet., 43, 768-775.
60. Huang, D.W., Sherman, B.T. and Lempicki, R.A. (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protocols, 4, 44-57.