Epigenomic Landscape of Melanoma Progression to Brain Metastasis: Unexplored Therapeutic Alternatives

References

• Bristow BN , CasilJ , SorvilloF , Basurto-DavilaR , KuoT . Melanoma-related mortality and productivity losses in the USA 1990–2008 . Melanoma Res.23 ( 4 ), 331 – 335 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Fidler IJ , SchackertG , ZhangRD , RadinskyR , FujimakiT . The biology of melanoma brain metastasis . Cancer Metastasis Rev.18 ( 3 ), 387 – 400 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Fidler IJ , BalasubramanianK , LinQ , KimSW , KimSJ . The brain microenvironment and cancer metastasis . Mol. Cells30 ( 2 ), 93 – 98 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Long GV , TrefzerU , DaviesMAet al. Dabrafenib in patients with Val600Glu or Val600Lys BRAF-mutant melanoma metastatic to the brain (BREAK-MB): a multicentre, open-label, Phase 2 trial . Lancet Oncol.13 ( 11 ), 1087 – 1095 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Harding JJ , CatalanottiF , MunhozRRet al. A retrospective evaluation of vemurafenib as treatment for BRAF-mutant melanoma brain metastases . Oncologist20 ( 7 ), 789 – 797 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Lawrence MS , StojanovP , PolakPet al. Mutational heterogeneity in cancer and the search for new cancer-associated genes . Nature499 ( 7457 ), 214 – 218 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Feinberg AP . Phenotypic plasticity and the epigenetics of human disease . Nature447 ( 7143 ), 433 – 440 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Karlic R , ChungHR , LasserreJ , VlahovicekK , VingronM . Histone modification levels are predictive for gene expression . Proc. Natl Acad. Sci. USA107 ( 7 ), 2926 – 2931 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Smith ZD , MeissnerA . DNA methylation: roles in mammalian development . Nat. Rev. Genet.14 ( 3 ), 204 – 220 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Chen T , DentSY . Chromatin modifiers and remodellers: regulators of cellular differentiation . Nat. Rev. Genet.15 ( 2 ), 93 – 106 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Holoch D , MoazedD . RNA-mediated epigenetic regulation of gene expression . Nat. Rev. Genet.16 ( 2 ), 71 – 84 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Valastyan S , WeinbergRA . Tumor metastasis: molecular insights and evolving paradigms . Cell147 ( 2 ), 275 – 292 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Arrowsmith CH , BountraC , FishPV , LeeK , SchapiraM . Epigenetic protein families: a new frontier for drug discovery . Nat. Rev. Drug Discov.11 ( 5 ), 384 – 400 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Ahuja N , EaswaranH , BaylinSB . Harnessing the potential of epigenetic therapy to target solid tumors . J. Clin. Invest.124 ( 1 ), 56 – 63 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Issa JP , KantarjianHM . Targeting DNA methylation . Clin. Cancer Res.15 ( 12 ), 3938 – 3946 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Marks PA , XuWS . Histone deacetylase inhibitors: potential in cancer therapy . J. Cell Biochem.107 ( 4 ), 600 – 608 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Nebbioso A , CarafaV , BenedettiR , AltucciL . Trials with ‘epigenetic’ drugs: an update . Mol. Oncol.6 ( 6 ), 657 – 682 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Xia C , Leon-FerreR , LauxDet al. Treatment of resistant metastatic melanoma using sequential epigenetic therapy (decitabine and panobinostat) combined with chemotherapy (temozolomide) . Cancer Chemother. Pharmacol.74 ( 4 ), 691 – 697 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Gonzalez-Gomez P , BelloMJ , AlonsoMEet al. Promoter methylation status of multiple genes in brain metastases of solid tumors . Int. J. Mol. Med.13 ( 1 ), 93 – 98 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Gonzalez-Gomez P , BelloMJ , AlonsoMEet al. Frequent death-associated protein-kinase promoter hypermethylation in brain metastases of solid tumors . Oncol. Rep.10 ( 4 ), 1031 – 1033 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Mezzanotte JJ , HillV , SchmidtMLet al. RASSF6 exhibits promoter hypermethylation in metastatic melanoma and inhibits invasion in melanoma cells . Epigenetics9 ( 11 ), 1496 – 1503 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Helmbold P , RichterAM , WaleschSet al. RASSF10 promoter hypermethylation is frequent in malignant melanoma of the skin but uncommon in nevus cell nevi . J. Invest. Dermatol.132 ( 3 Pt 1 ), 687 – 694 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Marzese DM , ScolyerRA , RoqueMet al. DNA methylation and gene deletion analysis of brain metastases in melanoma patients identifies mutually exclusive molecular alterations . Neuro Oncol.16 ( 11 ), 1499 – 1509 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Shabalin AA , AbergKA , van den OordEJ . Candidate gene methylation studies are at high risk of erroneous conclusions . Epigenomics7 ( 1 ), 13 – 15 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Marzese DM , HoonDS . Emerging technologies for studying DNA methylation for the molecular diagnosis of cancer . Expert Rev. Mol. Diagn.15 ( 5 ), 647 – 664 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Marzese DM , ScolyerRA , HuynhJLet al. Epigenome-wide DNA methylation landscape of melanoma progression to brain metastasis reveals aberrations on homeobox D cluster associated with prognosis . Hum. Mol. Genet.23 ( 1 ), 226 – 238 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Marzese DM , HuynhJL , KawasNP , HoonDS . Multi-platform genome-wide analysis of melanoma progression to brain metastasis . Genom. Data2 , 150 – 152 ( 2014 ).
   PubMedGoogle Scholar
• Chen YA , LemireM , ChoufaniSet al. Discovery of cross-reactive probes and polymorphic CpGs in the Illumina Infinium HumanMethylation450 microarray . Epigenetics8 ( 2 ), 203 – 209 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Barrow TM , ByunHM . Single nucleotide polymorphisms on DNA methylation microarrays: precautions against confounding . Epigenomics6 ( 6 ), 577 – 579 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Sandoval J , HeynH , MoranSet al. Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome . Epigenetics6 ( 6 ), 692 – 702 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Lister R , PelizzolaM , DowenRHet al. Human DNA methylomes at base resolution show widespread epigenomic differences . Nature462 ( 7271 ), 315 – 322 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Schroeder DI , LottP , KorfI , LasalleJM . Large-scale methylation domains mark a functional subset of neuronally expressed genes . Genome Res.21 ( 10 ), 1583 – 1591 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Nygaard V , PrasmickaiteL , VasiliauskaiteK , ClancyT , HovigE . Melanoma brain colonization involves the emergence of a brain-adaptive phenotype . Oncoscience1 ( 1 ), 82 – 94 ( 2014 ).
   PubMedGoogle Scholar
• Mori T , MartinezSR , O’DaySJet al. Estrogen receptor-alpha methylation predicts melanoma progression . Cancer Res.66 ( 13 ), 6692 – 6698 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Tanemura A , TerandoAM , SimMSet al. CpG island methylator phenotype predicts progression of malignant melanoma . Clin. Cancer Res.15 ( 5 ), 1801 – 1807 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Mori T , O’daySJ , UmetaniNet al. Predictive utility of circulating methylated DNA in serum of melanoma patients receiving biochemotherapy . J. Clin. Oncol.23 ( 36 ), 9351 – 9358 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Hemesath TJ , PriceER , TakemotoC , BadalianT , FisherDE . MAP kinase links the transcription factor Microphthalmia to c-Kit signalling in melanocytes . Nature391 ( 6664 ), 298 – 301 ( 1998 ).
   PubMed Web of Science ®Google Scholar
• Peres J , PrinceS . The T-box transcription factor, TBX3, is sufficient to promote melanoma formation and invasion . Mol. Cancer12 ( 1 ), 117 ( 2013 ).
   PubMedGoogle Scholar
• Besch R , BerkingC . POU transcription factors in melanocytes and melanoma . Eur. J. Cell Biol.93 ( 1–2 ), 55 – 60 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Venkatesh S , WorkmanJL . Histone exchange, chromatin structure and the regulation of transcription . Nat. Rev. Mol. Cell Biol.16 ( 3 ), 178 – 189 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• De Laat W , DubouleD . Topology of mammalian developmental enhancers and their regulatory landscapes . Nature502 ( 7472 ), 499 – 506 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Loven J , HokeHA , LinCYet al. Selective inhibition of tumor oncogenes by disruption of super-enhancers . Cell153 ( 2 ), 320 – 334 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Kapoor A , GoldbergMS , CumberlandLKet al. The histone variant macroH2A suppresses melanoma progression through regulation of CDK8 . Nature468 ( 7327 ), 1105 – 1109 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Vardabasso C , Gaspar-MaiaA , HassonDet al. Histone variant H2A.Z.2 mediates proliferation and drug sensitivity of malignant melanoma . Mol. Cell59 ( 1 ), 75 – 88 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Guo JU , MaDK , MoHet al. Neuronal activity modifies the DNA methylation landscape in the adult brain . Nat. Neurosci.14 ( 10 ), 1345 – 1351 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Wahl MC , WillCL , LuhrmannR . The spliceosome: design principles of a dynamic RNP machine . Cell136 ( 4 ), 701 – 718 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Marzese DM , LiuM , HuynhJLet al. Brain metastasis is predetermined in early stages of cutaneous melanoma by CD44v6 expression through epigenetic regulation of the spliceosome . Pigment Cell Melanoma Res.28 ( 1 ), 82 – 93 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Klein A , SchwartzH , Sagi-AssifOet al. Astrocytes facilitate melanoma brain metastasis via secretion of IL-23 . J. Pathol.236 ( 1 ), 116 – 127 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Klein-Goldberg A , MamanS , WitzIP . The role played by the microenvironment in site-specific metastasis . Cancer Lett.352 ( 1 ), 54 – 58 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Maman S , Edry-BotzerL , Sagi-AssifOet al. The metastatic microenvironment: lung-derived factors control the viability of neuroblastoma lung metastasis . Int. J. Cancer133 ( 10 ), 2296 – 2306 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Klein A , Sagi-AssifO , IzraelySet al. The metastatic microenvironment: brain-derived soluble factors alter the malignant phenotype of cutaneous and brain-metastasizing melanoma cells . Int. J. Cancer131 ( 11 ), 2509 – 2518 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Izraely S , Sagi-AssifO , KleinAet al. The metastatic microenvironment: brain-residing melanoma metastasis and dormant micrometastasis . Int. J. Cancer131 ( 5 ), 1071 – 1082 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Izraely S , KleinA , Sagi-AssifOet al. Chemokine-chemokine receptor axes in melanoma brain metastasis . Immunol. Lett.130 ( 1–2 ), 107 – 114 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Liz J , EstellerM . lncRNAs and microRNAs with a role in cancer development . Biochim. Biophys. Acta doi:10.1016/j.bbagrm.2015.06.015 ( 2015 ) ( Epub ahead of print ).
   PubMed Web of Science ®Google Scholar
• Mueller WC , SpectorY , EdmonstonTBet al. Accurate classification of metastatic brain tumors using a novel microRNA-based test . Oncologist16 ( 2 ), 165 – 174 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Hanniford D , ZhongJ , KoetzLet al. A miRNA-based signature detected in primary melanoma tissue predicts development of brain metastasis . Clin. Cancer Res. pii: clincanres.2566.2014 ( 2015 ) ( Epub ahead of print ).
   PubMed Web of Science ®Google Scholar
• Fleming NH , ZhongJ , da SilvaIPet al. Serum-based miRNAs in the prediction and detection of recurrence in melanoma patients . Cancer121 ( 1 ), 51 – 59 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Kung JT , ColognoriD , LeeJT . Long noncoding RNAs: past, present, and future . Genetics193 ( 3 ), 651 – 669 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Lessard L , LiuM , MarzeseDMet al. The CASC15 long intergenic non-coding RNA locus is involved in melanoma progression and phenotype-switching . J. Invest. Dermatol. doi:10.1038/jid.2015.200 ( 2015 ) ( Epub ahead of print ).
   PubMed Web of Science ®Google Scholar
• Eichler AF , ChungE , KodackDP , LoefflerJS , FukumuraD , JainRK . The biology of brain metastases-translation to new therapies . Nat. Rev. Clin. Oncol.8 ( 6 ), 344 – 356 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Timar J , GyorffyB , RasoE . Gene signature of the metastatic potential of cutaneous melanoma: too much for too little?Clin. Exp. Metastasis27 ( 6 ), 371 – 387 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Bucheit AD , ChenG , SiroyAet al. Complete loss of PTEN protein expression correlates with shorter time to brain metastasis and survival in stage IIIB/C melanoma patients with BRAFv600 mutations . Clin. Cancer Res.20 ( 21 ), 5527 – 5536 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Jilaveanu LB , ParisiF , BarrMLet al. PLEKHA5 as a biomarker and potential mediator of melanoma brain metastasis . Clin. Cancer Res.21 ( 9 ), 2138 – 2147 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Dzienis MR , AtkinsonVG . Response rate to vemurafenib in patients with B-RAF-positive melanoma brain metastases: a retrospective review . Melanoma Res.24 ( 4 ), 349 – 353 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Chen G , ChakravartiN , AardalenKet al. Molecular profiling of patient-matched brain and extracranial melanoma metastases implicates the PI3K pathway as a therapeutic target . Clin. Cancer Res.20 ( 21 ), 5537 – 5546 ( 2014 ).
   PubMed Web of Science ®Google Scholar