Integrative epigenomic analysis of differential DNA methylation in urothelial carcinoma

Genome Medicine

Volumn 7, Issue 1, 2015, Pages

  Aine, Mattias ^a   Sjödahl, Gottfrid ^b   Eriksson, Pontus ^a   Veerla, Srinivas ^a   Lindgren, David ^c   Ringnér, Markus ^a   Höglund, Mattias ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AGED; ARTICLE; CANCER PROGNOSIS; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC CONSERVATION; HETEROCHROMATIN; HUMAN; MAJOR CLINICAL STUDY; MALE; MUTATION RATE; NERVE CELL DIFFERENTIATION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; SOMATIC MUTATION; TRANSCRIPTION INITIATION SITE; TRANSITIONAL CELL CARCINOMA; TUMOR DIFFERENTIATION;

EID: 84925342343     PISSN: None     EISSN: 1756994X     Source Type: Journal    
DOI: 10.1186/s13073-015-0144-4     Document Type: Article

References (65)

1. Wu XR. Urothelial tumorigenesis: a tale of divergent pathways. Nat Rev Cancer. 2005;5:713-25.
2. Golub TR, Slonim DK, Tamayo P, Huard C, Gaasenbeek M, Mesirov JP, et al. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science. 1999;286:531-7.
3. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A. 2001;98:10869-74.
4. Sjodahl G, Lauss M, Lovgren K, Chebil G, Gudjonsson S, Veerla S, et al. A molecular taxonomy for urothelial carcinoma. Clin Cancer Res. 2012;18:3377-86.
5. Sjodahl G, Lovgren K, Lauss M, Patschan O, Gudjonsson S, Chebil G, et al. Toward a molecular pathologic classification of urothelial carcinoma. Am J Pathol. 2013;183:681-91.
6. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev Cancer. 2004;4:143-53.
7. Hinoue T, Weisenberger DJ, Lange CP, Shen H, Byun HM, Van Den Berg D, et al. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res. 2012;22:271-82.
8. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell. 2010;17:510-22.
9. Stransky N, Vallot C, Reyal F, Bernard-Pierrot I, de Medina SG, Segraves R, et al. Regional copy number-independent deregulation of transcription in cancer. Nat Genet. 2006;38:1386-96.
10. Vallot C, Stransky N, Bernard-Pierrot I, Herault A, Zucman-Rossi J, Chapeaublanc E, et al. A novel epigenetic phenotype associated with the most aggressive pathway of bladder tumor progression. J Natl Cancer Inst. 2011;103:47-60.
11. Lauss M, Aine M, Sjodahl G, Veerla S, Patschan O, Gudjonsson S, et al. DNA methylation analyses of urothelial carcinoma reveal distinct epigenetic subtypes and an association between gene copy number and methylation status. Epigenetics. 2012;7:858-67.
12. Balbas-Martinez C, Sagrera A, Carrillo-de-Santa-Pau E, Earl J, Marquez M, Vazquez M, et al. Recurrent inactivation of STAG2 in bladder cancer is not associated with aneuploidy. Nat Genet. 2013;45:1464-9.
13. Guo G, Sun X, Chen C, Wu S, Huang P, Li Z, et al. Whole-genome and whole-exome sequencing of bladder cancer identifies frequent alterations in genes involved in sister chromatid cohesion and segregation. Nat Genet. 2013;45:1459-63.
14. Gui Y, Guo G, Huang Y, Hu X, Tang A, Gao S, et al. Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nat Genet. 2011;43:875-8.
15. The Cancer Genome Atlas Network. Comprehensive molecular characterization of urothelial bladder carcinoma. Nature. 2014;507:315-22.
16. Kandimalla R, van Tilborg AA, Kompier LC, Stumpel DJ, Stam RW, Bangma CH, et al. Genome-wide analysis of CpG island methylation in bladder cancer identified TBX2, TBX3, GATA2, and ZIC4 as pTa-specific prognostic markers. Eur Urol. 2012;61:1245-56.
17. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature. 2011;473:43-9.
18. Lienert F, Wirbelauer C, Som I, Dean A, Mohn F, Schubeler D. Identification of genetic elements that autonomously determine DNA methylation states. Nat Genet. 2011;43:1091-7.
19. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 2006;20:1123-36.
20. 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.
21. Lindgren D, Frigyesi A, Gudjonsson S, Sjodahl G, Hallden C, Chebil G, et al. Combined gene expression and genomic profiling define two intrinsic molecular subtypes of urothelial carcinoma and gene signatures for molecular grading and outcome. Cancer Res. 2010;70:3463-72.
22. Cooper GM, Stone EA, Asimenos G, Green ED, Batzoglou S, Sidow A. Distribution and intensity of constraint in mammalian genomic sequence. Genome Res. 2005;15:901-13.
23. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125:315-26.
24. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell. 2006;125:301-13.
25. Sturm D, Witt H, Hovestadt V, Khuong-Quang DA, Jones DT, Konermann C, et al. Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell. 2012;22:425-37.
26. Landan G, Cohen NM, Mukamel Z, Bar A, Molchadsky A, Brosh R, et al. Epigenetic polymorphism and the stochastic formation of differentially methylated regions in normal and cancerous tissues. Nat Genet. 2012;44:1207-14.
27. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature. 2007;448:553-60.
28. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet. 2008;40:499-507.
29. Monti S, Tamayo P, Mesirov J, Golub T. Consensus clustering: a resampling-based method for class discovery and visualization of gene expression microarray data. Machine Learning. 2003;52:91-118.
30. The ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57-74.
31. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell. 2008;132:422-33.
32. Kundaje A, Kyriazopoulou-Panagiotopoulou S, Libbrecht M, Smith CL, Raha D, Winters EE, et al. Ubiquitous heterogeneity and asymmetry of the chromatin environment at regulatory elements. Genome Res. 2012;22:1735-47.
33. Robbins MJ, Michalovich D, Hill J, Calver AR, Medhurst AD, Gloger I, et al. Molecular cloning and characterization of two novel retinoic acid-inducible orphan G-protein-coupled receptors (GPRC5B and GPRC5C). Genomics. 2000;67:8-18.
34. Zirn B, Samans B, Spangenberg C, Graf N, Eilers M, Gessler M. All-trans retinoic acid treatment of Wilms tumor cells reverses expression of genes associated with high risk and relapse in vivo. Oncogene. 2005;24:5246-51.
35. Wang GG, Song J, Wang Z, Dormann HL, Casadio F, Li H, et al. Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature. 2009;459:847-51.
36. Schug TT, Berry DC, Shaw NS, Travis SN, Noy N. Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell. 2007;129:723-33.
37. Bunaciu RP, Yen A. Activation of the aryl hydrocarbon receptor AhR Promotes retinoic acid-induced differentiation of myeloblastic leukemia cells by restricting expression of the stem cell transcription factor Oct4. Cancer Res. 2011;71:2371-80.
38. Schuettengruber B, Martinez AM, Iovino N, Cavalli G. Trithorax group proteins: switching genes on and keeping them active. Nat Rev Mol Cell Biol. 2011;12:799-814.
39. Copur O, Muller J. The histone H3-K27 demethylase Utx regulates HOX gene expression in Drosophila in a temporally restricted manner. Development. 2013;140:3478-85.
40. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13:484-92.
41. Heyn H, Esteller M. DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet. 2012;13:679-92.
42. Wilhelm-Benartzi CS, Koestler DC, Houseman EA, Christensen BC, Wiencke JK, Schned AR, et al. DNA methylation profiles delineate etiologic heterogeneity and clinically important subgroups of bladder cancer. Carcinogenesis. 2010;31:1972-6.
43. Wolff EM, Chihara Y, Pan F, Weisenberger DJ, Siegmund KD, Sugano K, et al. Unique DNA methylation patterns distinguish noninvasive and invasive urothelial cancers and establish an epigenetic field defect in premalignant tissue. Cancer Res. 2010;70:8169-78.
44. Reinert T, Modin C, Castano FM, Lamy P, Wojdacz TK, Hansen LL, et al. Comprehensive genome methylation analysis in bladder cancer: identification and validation of novel methylated genes and application of these as urinary tumor markers. Clin Cancer Res. 2011;17:5582-92.
45. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 2009;462:315-22.
46. Pan G, Tian S, Nie J, Yang C, Ruotti V, Wei H, et al. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell. 2007;1:299-312.
47. Weissman AM. How much REST is enough? Cancer Cell. 2008;13:381-3.
48. Coulson JM. Transcriptional regulation: cancer, neurons and the REST. Curr Biol. 2005;15:R665-8.
49. Westbrook TF, Martin ES, Schlabach MR, Leng Y, Liang AC, Feng B, et al. A genetic screen for candidate tumor suppressors identifies REST. Cell. 2005;121:837-48.
50. Lunyak VV, Burgess R, Prefontaine GG, Nelson C, Sze SH, Chenoweth J, et al. Corepressor-dependent silencing of chromosomal regions encoding neuronal genes. Science. 2002;298:1747-52.
51. Arnold P, Scholer A, Pachkov M, Balwierz PJ, Jorgensen H, Stadler MB, et al. Modeling of epigenome dynamics identifies transcription factors that mediate Polycomb targeting. Genome Res. 2013;23:60-73.
52. Peric-Hupkes D, van Steensel B. Linking cohesin to gene regulation. Cell. 2008;132:925-8.
53. McLellan JL, O'Neil NJ, Barrett I, Ferree E, van Pel DM, Ushey K, et al. Synthetic lethality of cohesins with PARPs and replication fork mediators. PLoS Genet. 2012;8:e1002574.
54. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet. 2009;41:178-86.
55. Slieker RC, Bos SD, Goeman JJ, Bovee JV, Talens RP, van der Breggen R, et al. Identification and systematic annotation of tissue-specific differentially methylated regions using the Illumina 450k array. Epigenetics Chromatin. 2013;6:26.
56. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485:376-80.
57. Gandhi D, Molotkov A, Batourina E, Schneider K, Dan H, Reiley M, et al. Retinoid signaling in progenitors controls specification and regeneration of the urothelium. Dev Cell. 2013;26:469-82.
58. Mauney JR, Ramachandran A, Yu RN, Daley GQ, Adam RM, Estrada CR. All-trans retinoic acid directs urothelial specification of murine embryonic stem cells via GATA4/6 signaling mechanisms. PLoS One. 2010;5:e11513.
59. Huang L, Pu Y, Hepps D, Danielpour D, Prins GS. Posterior Hox gene expression and differential androgen regulation in the developing and adult rat prostate lobes. Endocrinology. 2007;148:1235-45.
60. Taylor HS, Vanden Heuvel GB, Igarashi P. A conserved Hox axis in the mouse and human female reproductive system: late establishment and persistent adult expression of the Hoxa cluster genes. Biol Reprod. 1997;57:1338-45.
61. Agger K, Cloos PA, Christensen J, Pasini D, Rose S, Rappsilber J, et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature. 2007;449:731-4.
62. Lan F, Bayliss PE, Rinn JL, Whetstine JR, Wang JK, Chen S, et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature. 2007;449:689-94.
63. Van Batavia J, Yamany T, Molotkov A, Dan H, Mansukhani M, Batourina E, et al. Bladder cancers arise from distinct urothelial sub-populations. Nat Cell Biol. 2014;16:982-91.
64. Shin K, Lim A, Odegaard JI, Honeycutt JD, Kawano S, Hsieh MH, et al. Cellular origin of bladder neoplasia and tissue dynamics of its progression to invasive carcinoma. Nat Cell Biol. 2014;16:469-78.
65. Shin K, Lee J, Guo N, Kim J, Lim A, Qu L, et al. Hedgehog/Wnt feedback supports regenerative proliferation of epithelial stem cells in bladder. Nature. 2011;472:110-4.