DNA-Methylome Analysis of Mouse Intestinal Adenoma Identifies a Tumour-Specific Signature That Is Partly Conserved in Human Colon Cancer

PLoS Genetics

Volumn 9, Issue 2, 2013, Pages

  Grimm, Christina ^a,b   Chavez, Lukas ^a   Vilardell, Mireia ^a   Farrall, Alexandra L ^a   Tierling, Sascha ^c   Böhm, Julia W ^c   Grote, Phillip ^a   Lienhard, Matthias ^a   Dietrich, Jörn ^a   Timmermann, Bernd ^a   Walter, Jörn ^c   Schweiger, Michal R ^a   Lehrach, Hans ^a   Herwig, Ralf ^a   Herrmann, Bernhard G ^a,b   Morkel, Markus ^a,b  

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; DNA; DNA METHYLTRANSFERASE; POLYCOMB GROUP PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2;

ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL EXPANSION; COLON ADENOMA; COLON CANCER; CONTROLLED STUDY; CRYPT CELL; DNA METHYLATION; EPIGENETICS; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; INTESTINAL STEM CELL; MOUSE; NONHUMAN; PROMOTER REGION; STEM CELL; TUMOR CELL; TUMOR SUPPRESSOR GENE; UPREGULATION;

ADENOMA; ANIMALS; BASE SEQUENCE; COLONIC NEOPLASMS; CPG ISLANDS; DNA METHYLATION; EPIGENOMICS; GENOME; HUMANS; INTESTINAL NEOPLASMS; MICE; POLYCOMB-GROUP PROTEINS; SYNTENY;

EID: 84874774770     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003250     Document Type: Article

References (60)

1. Margueron R, Reinberg D, (2010) Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet 11: 285-296 doi:10.1038/nrg2752.
2. Cedar H, Bergman Y, (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 10: 295-304 doi:10.1038/nrg2540.
3. Lund AH, van Lohuizen M, (2004) Polycomb complexes and silencing mechanisms. Curr Opin Cell Biol 16: 239-246 doi:10.1016/j.ceb.2004.03.010.
4. Viré E, Brenner C, Deplus R, Blanchon L, Fraga M, et al. (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439: 871-874 doi:10.1038/nature04431.
5. Razin A, Shemer R, (1995) DNA methylation in early development. Hum Mol Genet 4 Spec No: 1751-1755.
6. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, et al. (2005) Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet 37: 853-862 doi:10.1038/ng1598.
7. Keshet I, Schlesinger Y, Farkash S, Rand E, Hecht M, et al. (2006) Evidence for an instructive mechanism of de novo methylation in cancer cells. Nat Genet 38: 149-153 doi:10.1038/ng1719.
8. Jia D, Jurkowska RZ, Zhang X, Jeltsch A, Cheng X, (2007) Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449: 248-251 doi:10.1038/nature06146.
9. Ooi SKT, Qiu C, Bernstein E, Li K, Jia D, et al. (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448: 714-717 doi:10.1038/nature05987.
10. Jones PA, Baylin SB, (2007) The epigenomics of cancer. Cell 128: 683-692 doi:10.1016/j.cell.2007.01.029.
11. Esteller M, (2008) Epigenetics in cancer. N Engl J Med 358: 1148-1159 doi:10.1056/NEJMra072067.
12. Baylin SB, (2009) Stem cells, cancer, and epigenetics. StemBook pp. 1-14 doi:10.3824/stembook.1.50.1.
13. Jones PA, Baylin SB, (2002) The fundamental role of epigenetic events in cancer. Nat Rev Genet 3: 415-428 doi:10.1038/nrg816.
14. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, et al. (2007) Epigenetic stem cell signature in cancer. Nat Genet 39: 157-158 doi:10.1038/ng1941.
15. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, et al. (2007) Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 39: 232-236 doi:10.1038/ng1950.
16. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, et al. (2007) A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 39: 237-242 doi:10.1038/ng1972.
17. Zhuang J, Jones A, Lee S-H, Ng E, Fiegl H, et al. (2012) The dynamics and prognostic potential of DNA methylation changes at stem cell gene loci in women's cancer. PLoS Genet 8: e1002517 doi:10.1371/journal.pgen.1002517.
18. Easwaran H, Johnstone SE, Van Neste L, Ohm J, Mosbruger T, et al. (2012) A DNA hypermethylation module for the stem/progenitor cell signature of cancer. Genome Res 22: 837-849 doi:10.1101/gr.131169.111.
19. Sparmann A, van Lohuizen M, (2006) Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 6: 846-856 doi:10.1038/nrc1991.
20. Mills AA, (2010) Throwing the cancer switch: reciprocal roles of polycomb and trithorax proteins. Nat Rev Cancer 10: 669-682 doi:10.1038/nrc2931.
21. Schuettengruber B, Martinez A-M, Iovino N, Cavalli G, (2011) Trithorax group proteins: switching genes on and keeping them active. Nat Rev Mol Cell Biol 12: 799-814 doi:10.1038/nrm3230.
22. Fearon ER, Vogelstein B, (1990) A genetic model for colorectal tumorigenesis. Cell 61: 759-767.
23. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, et al. (1992) Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 256: 668-670.
24. Esteller M, (2007) Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet 8: 286-298 doi:10.1038/nrg2005.
25. Lao VV, Grady WM, (2011) Epigenetics and colorectal cancer. Nat Rev Gastroenterol Hepatol doi:10.1038/nrgastro.2011.173.
26. Down TA, Rakyan VK, Turner DJ, Flicek P, Li H, et al. (2008) A Bayesian deconvolution strategy for immunoprecipitation-based DNA methylome analysis. Nat Biotechnol 26: 779-785 doi:10.1038/nbt1414.
27. Chavez L, Jozefczuk J, Grimm C, Dietrich J, Timmermann B, et al. (2010) Computational analysis of genome-wide DNA methylation during the differentiation of human embryonic stem cells along the endodermal lineage. Genome Res 20: 1441-1450 doi:10.1101/gr.110114.110.
28. Estécio MRH, Gharibyan V, Shen L, Ibrahim AEK, Doshi K, et al. (2007) LINE-1 hypomethylation in cancer is highly variable and inversely correlated with microsatellite instability. PLoS ONE 2: e399 doi:10.1371/journal.pone.0000399.
29. Sunami E, de Maat M, Vu A, Turner RR, Hoon DSB, (2011) LINE-1 hypomethylation during primary colon cancer progression. PLoS ONE 6: e18884 doi:10.1371/journal.pone.0018884.
30. El-Maarri O, (2004) SIRPH analysis: SNuPE with IP-RP-HPLC for quantitative measurements of DNA methylation at specific CpG sites. Methods Mol Biol 287: 195-205 doi:10.1385/1-59259-828-5:195.
31. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353 doi:10.1038/nature04733.
32. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, et al. (2008) An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 40: 499-507 doi:10.1038/ng.127.
33. Guenther MG, Lawton LN, Rozovskaia T, Frampton GM, Levine SS, et al. (2008) Aberrant chromatin at genes encoding stem cell regulators in human mixed-lineage leukemia. Genes Dev 22: 3403-3408 doi:10.1101/gad.1741408.
34. Williams K, Christensen J, Pedersen MT, Johansen JV, Cloos PAC, et al. (2011) TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473: 343-348 doi:10.1038/nature10066.
35. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102: 15545-15550 doi:10.1073/pnas.0506580102.
36. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, et al. (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457: 608-611 doi:10.1038/nature07602.
37. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, et al. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007 doi:10.1038/nature06196.
38. Dietrich WF, Lander ES, Smith JS, Moser AR, Gould KA, et al. (1993) Genetic identification of Mom-1, a major modifier locus affecting Min-induced intestinal neoplasia in the mouse. Cell 75: 631-639.
39. Hlubek F, Brabletz T, Budczies J, Pfeiffer S, Jung A, et al. (2007) Heterogeneous expression of Wnt/beta-catenin target genes within colorectal cancer. Int J Cancer 121: 1941-1948 doi:10.1002/ijc.22916.
40. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, et al. (2010) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469: 415 doi:10.1038/nature09637.
41. Merlos-Suárez A, Barriga FM, Jung P, Iglesias M, Céspedes MV, et al. (2011) The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 8: 511-524 doi:10.1016/j.stem.2011.02.020.
42. Farrall AL, Riemer P, Leushacke M, Sreekumar A, Grimm C, et al. (2012) Wnt and BMP signals control intestinal adenoma cell fates. Int J Cancer doi:10.1002/ijc.27500.
43. Li QL, Ito K, Sakakura C, Fukamachi H, Inoue KI, et al. (2002) Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 109: 113-124.
44. Nishio M, Sakakura C, Nagata T, Komiyama S, Miyashita A, et al. (2010) RUNX3 promoter methylation in colorectal cancer: its relationship with microsatellite instability and its suitability as a novel serum tumor marker. Anticancer Res 30: 2673-2682.
45. Tanaka K, Imoto I, Inoue J, Kozaki K, Tsuda H, et al. (2007) Frequent methylation-associated silencing of a candidate tumor-suppressor, CRABP1, in esophageal squamous-cell carcinoma. Oncogene 26: 6456-6468 doi:10.1038/sj.onc.1210459.
46. Gaspar C, Cardoso J, Franken P, Molenaar L, Morreau H, et al. (2008) Cross-species comparison of human and mouse intestinal polyps reveals conserved mechanisms in adenomatous polyposis coli (APC)-driven tumorigenesis. Am J Pathol 172: 1363-1380 doi:10.2353/ajpath.2008.070851.
47. Jin B, Yao B, Li J-L, Fields CR, Delmas AL, et al. (2009) DNMT1 and DNMT3B modulate distinct polycomb-mediated histone modifications in colon cancer. Cancer Res 69: 7412-7421 doi:10.1158/0008-5472.CAN-09-0116.
48. Fackler MJ, Umbricht CB, Williams D, Argani P, Cruz L-A, 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 doi:10.1158/0008-5472.CAN-11-1630.
49. Peterziel H, Müller J, Danner A, Barbus S, Liu H-K, et al. (2012) Expression of podoplanin in human astrocytic brain tumors is controlled by the PI3K-AKT-AP-1 signaling pathway and promoter methylation. Neuro-oncology 14: 426-439 doi:10.1093/neuonc/nos055.
50. Izumi H, Inoue J, Yokoi S, Hosoda H, Shibata T, et al. (2005) Frequent silencing of DBC1 is by genetic or epigenetic mechanisms in non-small cell lung cancers. Hum Mol Genet 14: 997-1007 doi:10.1093/hmg/ddi092.
51. Luxen S, Belinsky SA, Knaus UG, (2008) Silencing of DUOX NADPH oxidases by promoter hypermethylation in lung cancer. Cancer Res 68: 1037-1045 doi:10.1158/0008-5472.CAN-07-5782.
52. Miotto E, Sabbioni S, Veronese A, Calin GA, Gullini S, et al. (2004) Frequent aberrant methylation of the CDH4 gene promoter in human colorectal and gastric cancer. Cancer Res 64: 8156-8159 doi:10.1158/0008-5472.CAN-04-3000.
53. Haruki S, Imoto I, Kozaki K-I, Matsui T, Kawachi H, et al. (2010) Frequent silencing of protocadherin 17, a candidate tumour suppressor for esophageal squamous cell carcinoma. Carcinogenesis 31: 1027-1036 doi:10.1093/carcin/bgq053.
54. Lind GE, Kleivi K, Meling GI, Teixeira MR, Thiis-Evensen E, et al. (2006) ADAMTS1, CRABP1, and NR3C1 identified as epigenetically deregulated genes in colorectal tumorigenesis. Cell Oncol 28: 259-272.
55. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, et al. (2008) Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454: 766-770 doi:10.1038/nature07107.
56. Halberg RB, Waggoner J, Rasmussen K, White A, Clipson L, et al. (2009) Long-lived Min mice develop advanced intestinal cancers through a genetically conservative pathway. Cancer Res 69: 5768-5775 doi:10.1158/0008-5472.CAN-09-0446.
57. Sato T, Stange DE, Ferrante M, Vries RGJ, van Es JH, et al. (2011) Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141: 1762-1772 doi:10.1053/j.gastro.2011.07.050.
58. Grimm C, Adjaye J, (2012) Analysis of the methylome of human embryonic stem cells employing methylated DNA immunoprecipitation coupled to next-generation sequencing. Methods Mol Biol 873: 281-295 doi:10.1007/978-1-61779-794-1_19.
59. Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, et al. (2009) Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 37: e123 doi:10.1093/nar/gkp596.
60. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, et al. (2011) The UCSC Genome Browser database: update 2011. Nucleic Acids Res 39: D876-D882 doi:10.1093/nar/gkq963.