Methylation-dependent SOX9 expression mediates invasion in human melanoma cells and is a negative prognostic factor in advanced melanoma

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Cheng, Phil F ^a   Shakhova, Olga ^b   Widmer, Daniel S ^a   Eichhoff, Ossia M ^a   Zingg, Daniel ^b   Frommel, Sandra C ^b   Belloni, Benedetta ^a   Raaijmakers, Marieke I G ^a   Goldinger, Simone M ^a   Santoro, Raffaella ^b   Hemmi, Silvio ^b   Sommer, Lukas ^b   Dummer, Reinhard ^a   Levesque, Mitchell P ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SOX9; SOX9 PROTEIN, HUMAN;

ADVANCED CANCER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER PROGNOSIS; CANCER SURVIVAL; CARCINOGENESIS; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENOME ANALYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MELANOMA; MELANOMA CELL LINE; METASTASIS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; ONCOGENE; PROMOTER REGION; PROTEIN DNA BINDING; SIGNAL TRANSDUCTION; SOX9 GENE; SURVIVAL RATE; TUMOR INVASION; AGED; ANIMAL; BIOSYNTHESIS; CANCER STAGING; GENE EXPRESSION REGULATION; GENETICS; MIDDLE AGED; PATHOLOGY; PROGNOSIS; SKIN TUMOR; SURVIVAL; TUMOR CELL LINE;

AGED; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; DNA METHYLATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MELANOMA; MICE; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PROGNOSIS; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; SOX9 TRANSCRIPTION FACTOR; SURVIVAL ANALYSIS;

EID: 84928328205     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0594-4     Document Type: Article

References (58)

1. Dupin E, Le Douarin NM. Development of melanocyte precursors from the vertebrate neural crest. Oncogene. 2003;22:3016-23.
2. Garbe C, Leiter U. Melanoma epidemiology and trends. Clin Dermatol. 2009;27:3-9.
3. MacKie RM, Hauschild A, Eggermont AM. Epidemiology of invasive cutaneous melanoma. Ann Oncol. 2009;20:vi1-7.
4. Quintana E, Shackleton M, Foster HR, Fullen DR, Sabel MS, Johnson TM, et al. Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell. 2010;18:510-23.
5. Perego M, Tortoreto M, Tragni G, Mariani L, Deho P, Carbone A, et al. Heterogeneous phenotype of human melanoma cells with in vitro and in vivo features of tumor-initiating cells. J Invest Dermatol. 2010;130:1877-86.
6. Roesch A, Fukunaga-Kalabis M, Schmidt EC, Zabierowski SE, Brafford PA, Vultur A, et al. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell. 2010;141:583-94.
7. Landsberg J, Kohlmeyer J, Renn M, Bald T, Rogava M, Cron M, et al. Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation. Nature. 2012;490:412-6.
8. Romano E, Schwartz GK, Chapman PB, Wolchock JD, Carvajal RD. Treatment implications of the emerging molecular classification system for melanoma. Lancet Oncol. 2011;12:913-22.
9. Hoek KS, Goding CR. Cancer stem cells versus phenotype-switching in melanoma. Pigment Cell Melanoma Res. 2010;23:746-59.
10. Freedman JA, Tyler DS, Nevins JR, Augustine CK. Use of gene expression and pathway signatures to characterize the complexity of human melanoma. Am J Pathol. 2011;178:2513-22.
11. Hoek KS, Schlegel NC, Brafford P, Sucker A, Ugurel S, Kumar R, et al. Metastatic potential of melanomas defined by specific gene expression profiles with no BRAF signature. Pigment Cell Res. 2006;19:290-302.
12. Hendrix MJ, Seftor EA, Seftor RE, Kasemeier-Kulesa J, Kulesa PM, Postovit LM. Reprogramming metastatic tumour cells with embryonic microenvironments. Nat Rev Cancer. 2007;7:246-55.
13. Widmer DS, Cheng PF, Eichhoff OM, Belloni BC, Zipser MC, Schlegel NC, et al. Systematic classification of melanoma cells by phenotype-specific gene expression mapping. Pigment Cell Melanoma Res. 2012;25:343-53.
14. Eichhoff OM, Zipser MC, Xu M, Weeraratna AT, Mihic D, Dummer R, et al. The immunohistochemistry of invasive and proliferative phenotype switching in melanoma: a case report. Melanoma Res. 2010;20:349-55.
15. Widmer DS, Hoek KS, Cheng PF, Eichhoff OM, Biedermann T, Raaijmakers MI, et al. Hypoxia contributes to melanoma heterogeneity by triggering HIF1alpha-dependent phenotype switching. J Invest Dermatol. 2013;133:2436-43.
16. Carreira S, Goodall J, Denat L, Rodriguez M, Nuciforo P, Hoek KS, et al. Mitf regulation of Dia1 controls melanoma proliferation and invasiveness. Genes Dev. 2006;20:3426-39.
17. Cheli Y, Giuliano S, Botton T, Rocchi S, Hofman V, Hofman P, et al. Mitf is the key molecular switch between mouse or human melanoma initiating cells and their differentiated progeny. Oncogene. 2011;30:2307-18.
18. Goodall J, Carreira S, Denat L, Kobi D, Davidson I, Nuciforo P, et al. Brn-2 represses microphthalmia-associated transcription factor expression and marks a distinct subpopulation of microphthalmia-associated transcription factor-negative melanoma cells. Cancer Res. 2008;68:7788-94.
19. Plass C. Cancer epigenomics. Hum Mol Genet. 2002;11:2479-88.
20. Baylin SB, Jones PA. A decade of exploring the cancer epigenome - biological and translational implications. Nat Rev Cancer. 2011;11:726-34.
21. Hansen KD, Timp W, Bravo HC, Sabunciyan S, Langmead B, McDonald OG, et al. Increased methylation variation in epigenetic domains across cancer types. Nat Genet. 2011;43:768-75.
22. Molognoni F, Cruz AT, Meliso FM, Morais AS, Souza CF, Xander P, et al. Epigenetic reprogramming as a key contributor to melanocyte malignant transformation. Epigenetics. 2011;6:450-64.
23. Sigalotti L, Coral S, Nardi G, Spessotto A, Cortini E, Cattarossi I, et al. Promoter methylation controls the expression of MAGE2, 3 and 4 genes in human cutaneous melanoma. J Immunother. 2002;25:16-26.
24. Nguyen T, Kuo C, Nicholl MB, Sim MS, Turner RR, Morton DL, et al. Downregulation of microRNA-29c is associated with hypermethylation of tumor-related genes and disease outcome in cutaneous melanoma. Epigenetics. 2011;6:388-94.
25. Deng T, Kuang Y, Wang L, Li J, Wang Z, Fei J. An essential role for DNA methyltransferase 3a in melanoma tumorigenesis. Biochem Biophys Res Commun. 2009;387:611-6.
26. Schinke C, Mo Y, Yu Y, Amiri K, Sosman J, Greally J, et al. Aberrant DNA methylation in malignant melanoma. Melanoma Res. 2010;20:253-65.
27. Alcazar O, Achberger S, Aldrich W, Hu Z, Negrotto S, Saunthararajah Y, et al. Epigenetic regulation by decitabine of melanoma differentiation in vitro and in vivo. Int J Cancer. 2012;131:18-29.
28. Cheung M, Briscoe J. Neural crest development is regulated by the transcription factor Sox9. Development. 2003;130:5681-93.
29. Passeron T, Valencia JC, Namiki T, Vieira WD, Passeron H, Miyamura Y, et al. Upregulation of SOX9 inhibits the growth of human and mouse melanomas and restores their sensitivity to retinoic acid. J Clin Invest. 2009;119:954-63.
30. Hoek KS, Eichhoff OM, Schlegel NC, Dobbeling U, Kobert N, Schaerer L, et al. In vivo switching of human melanoma cells between proliferative and invasive states. Cancer Res. 2008;68:650-6.
31. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, et al. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet. 2005;37:853-62.
32. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:Article3.
33. Passeron T, Valencia JC, Bertolotto C, Hoashi T, Le Pape E, Takahashi K, et al. SOX9 is a key player in ultraviolet B-induced melanocyte differentiation and pigmentation. Proc Natl Acad Sci U S A. 2007;104:13984-9.
34. Cook AL, Smith AG, Smit DJ, Leonard JH, Sturm RA. Co-expression of SOX9 and SOX10 during melanocytic differentiation in vitro. Exp Cell Res. 2005;308:222-35.
35. Eichhoff OM, Weeraratna A, Zipser MC, Denat L, Widmer DS, Xu M, et al. Differential LEF1 and TCF4 expression is involved in melanoma cell phenotype switching. Pigment Cell Melanoma Res. 2011;24:631-42.
36. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, et al. SOX9 directly regulates the type-II collagen gene. Nat Genet. 1997;16:174-8.
37. Shakhova O, Cheng P, Mishra PJ, Zingg D, Schaefer SM, Debbache J, et al. Antagonistic cross-regulation between Sox9 and Sox10 controls an anti-tumorigenic program in Melanoma. PLoS Genet. 2015;11:e1004877.
38. Mihic-Probst D, Ikenberg K, Tinguely M, Schraml P, Behnke S, Seifert B, et al. Tumor cell plasticity and angiogenesis in human melanomas. PLoS One. 2012;7:e33571.
39. Hendrix MJ, Seftor EA, Hess AR, Seftor RE. Molecular plasticity of human melanoma cells. Oncogene. 2003;22:3070-5.
40. Zipser MC, Eichhoff OM, Widmer DS, Schlegel NC, Schoenewolf NL, Stuart D, et al. A proliferative melanoma cell phenotype is responsive to RAF/MEK inhibition independent of BRAF mutation status. Pigment Cell Melanoma Res. 2011;24:326-33.
41. Fraga MF, Herranz M, Espada J, Ballestar E, Paz MF, Ropero S, et al. A mouse skin multistage carcinogenesis model reflects the aberrant DNA methylation patterns of human tumors. Cancer Res. 2004;64:5527-34.
42. Bonazzi VF, Nancarrow DJ, Stark MS, Moser RJ, Boyle GM, Aoude LG, et al. Cross-platform array screening identifies COL1A2, THBS1, TNFRSF10D and UCHL1 as genes frequently silenced by methylation in melanoma. PLoS One. 2011;6:e26121.
43. Koga Y, Pelizzola M, Cheng E, Krauthammer M, Sznol M, Ariyan S, et al. Genome-wide screen of promoter methylation identifies novel markers in melanoma. Genome Res. 2009;19:1462-70.
44. Muthusamy V, Duraisamy S, Bradbury CM, Hobbs C, Curley DP, Nelson B, et al. Epigenetic silencing of novel tumor suppressors in malignant melanoma. Cancer Res. 2006;66:11187-93.
45. Conway K, Edmiston SN, Khondker ZS, Groben PA, Zhou X, Chu H, et al. DNA-methylation profiling distinguishes malignant melanomas from benign nevi. Pigment Cell Melanoma Res. 2011;24:352-60.
46. Lian CG, Xu Y, Ceol C, Wu F, Larson A, Dresser K, et al. Loss of 5-hydroxymethylcytosine is an epigenetic hallmark of melanoma. Cell. 2012;150:1135-46.
47. Rajasekaran K, Kumar P, Schuldt KM, Peterson EJ, Vanhaesebroeck B, Dixit V, et al. Signaling by Fyn-ADAP via the Carma1-Bcl-10-MAP3K7 signalosome exclusively regulates inflammatory cytokine production in NK cells. Nat Immunol. 2013;14:1127-36.
48. Peres J, Prince S. The T-box transcription factor, TBX3, is sufficient to promote melanoma formation and invasion. Mol Cancer. 2013;12:117.
49. Rodriguez M, Aladowicz E, Lanfrancone L, Goding CR. Tbx3 represses E-cadherin expression and enhances melanoma invasiveness. Cancer Res. 2008;68:7872-81.
50. Raaijmakers MIG, Widmer DS, Maudrich M, Koch T, Langer A, Flace A, et al. A new live cell biobank workflow efficiently recovers heterogeneous melanoma cells from native biopsies. Exp Dermatol. 2015.
51. Geertsen RC, Hofbauer GF, Yue FY, Manolio S, Burg G, Dummer R. Higher frequency of selective losses of HLA-A and -B allospecificities in metastasis than in primary melanoma lesions. J Invest Dermatol. 1998;111:497-502.
52. Bock C, Reither S, Mikeska T, Paulsen M, Walter J, Lengauer T. BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics. 2005;21:4067-8.
53. Smyth GK. Limma: linear models for microarray data. New York: Springer; 2005.
54. Santoro R. Analysis of chromatin composition of repetitive sequences: the ChIP-Chop assay. Methods Mol Biol. 2014;1094:319-28.
55. Kadaja M, Keyes BE, Lin M, Pasolli HA, Genander M, Polak L, et al. SOX9: a stem cell transcriptional regulator of secreted niche signaling factors. Genes Dev. 2014;28:328-41.
56. Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, Arenillas DJ, et al. JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 2014;42:D142-7.
57. Therneau TM: A Package for Survival Analysis in S. In R package version 237-4; 2013.
58. Aryee MJ, Jaffe AE, Corrada-Bravo H, Ladd-Acosta C, Feinberg AP, Hansen KD, et al. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics. 2014;30:1363-9.