Genome architecture marked by retrotransposons modulates predisposition to DNA methylation in cancer

Genome Research

Volumn 20, Issue 10, 2010, Pages 1369-1382

  Estécio, Marcos R H ^a   Gallegos, Juan ^a   Vallot, Céline ^b   Castoro, Ryan J ^a   Chung, Woonbok ^a   Maegawa, Shinji ^a   Oki, Yasuhiro ^c   Kondo, Yutaka ^c   Jelinek, Jaroslav ^a   Shen, Lanlan ^d   Hartung, Helge ^e   Aplan, Peter D ^e   Czerniak, Bogdan A ^a   Liang, Shoudan ^a   Issa, Jean Pierre J ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b INSTITUT CURIE   (France)

^c AICHI CANCER CENTER HOSPITAL   (Japan)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CANCER CELL CULTURE; CANCER GENETICS; CARCINOGENESIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DEVELOPMENTAL STAGE; DNA METHYLATION; FEMALE; GENE FREQUENCY; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC PREDISPOSITION; GENOMICS; HUMAN; HUMAN CELL; HUMAN GENETICS; MALE; MARKER GENE; MOLECULAR MODEL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR DOWN REGULATION; RETROPOSON; TRANSCRIPTION INITIATION SITE; UNINDEXED SEQUENCE;

CELL LINE, TUMOR; DNA METHYLATION; EPIGENOMICS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENOME, HUMAN; HUMANS; LEUKEMIA, MYELOID, ACUTE; NEOPLASMS; RETROELEMENTS; TUMOR CELLS, CULTURED; URINARY BLADDER NEOPLASMS;

EID: 78649274945     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.107318.110     Document Type: Article

References (50)

1. Allen E, Horvath S, Tong F, Kraft P, Spiteri E, Riggs AD, Marahrens Y. 2003. High concentrations of long interspersed nuclear element sequence distinguish monoallelically expressed genes. Proc Natl Acad Sci 100: 9940-9945. (Pubitemid 37087047)
2. Al-Shahrour F, Minguez P, Tarraga J, Montaner D, Alloza E, Vaquerizas JM, Conde L, Blaschke C, Vera J, Dopazo J. 2006. BABELOMICS: A systems biology perspective in the functional annotation of genome-scale experiments. Nucleic Acids Res 34: W472-W476.
3. Arnaud P, Goubely C, Pelissier T, Deragon JM. 2000. SINE retroposons can be used in vivo as nucleation centers for de novo methylation. Mol Cell Biol 20: 3434-3441.
4. Baylin S, Bestor TH. 2002. Altered methylation patterns in cancer cell genomes: Cause or consequence? Cancer Cell 1: 299-305.
5. Bell AC, West AG, Felsenfeld G. 1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98: 387-396.
6. Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ, McMahon S, Karlsson EK, Kulbokas EJ III, Gingeras TR, et al. 2005. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120: 169-181.
7. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
8. Bock C, Paulsen M, Tierling S, Mikeska T, Lengauer T, Walter J. 2006. CpG island methylation in human lymphocytes is highly correlated with DNA sequence, repeats, and predicted DNA structure. PLoS Genet 2: e26. doi: 10.1371/journal.pgen.0020026.
9. Chen SS, Raval A, Johnson AJ, Hertlein E, Liu TH, Jin VX, Sherman MH, Liu SJ, Dawson DW, Williams KE, et al. 2009. Epigenetic changes during disease progression in a murine model of human chronic lymphocytic leukemia. Proc Natl Acad Sci 106: 13433-13438.
10. Choi CW, Chung YJ, Slape C, Aplan PD. 2008. Impaired differentiation and apoptosis of hematopoietic precursors in a mouse model of myelodysplastic syndrome. Haematologica 93: 1394-1397.
11. Das R, Dimitrova N, Xuan Z, Rollins RA, Haghighi F, Edwards JR, Ju J, Bestor TH, Zhang MQ. 2006. Computational prediction of methylation status in human genomic sequences. Proc Natl Acad Sci 103: 10713-10716. (Pubitemid 44078042)
12. Estecio MR, Youssef EM, Rahal P, Fukuyama EE, Gois-Filho JF, Maniglia JV, Goloni-Bertollo EM, Issa JP, Tajara EH. 2006. LHX6 is a sensitive methylation marker in head and neck carcinomas. Oncogene 25: 5018-5026.
13. Estecio MR, Yan PS, Ibrahim AE, Tellez CS, Shen L, Huang TH, Issa JP. 2007. High-throughput methylation profiling by MCA coupled to CpG island microarray. Genome Res 17: 1529-1536.
14. Faulkner GJ, Kimura Y, Daub CO, Wani S, Plessy C, Irvine KM, Schroder K, Cloonan N, Steptoe AL, Lassmann T, et al. 2009. The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 41: 563-571.
15. Feltus FA, Lee EK, Costello JF, Plass C, Vertino PM. 2003. Predicting aberrant CpG island methylation. Proc Natl Acad Sci 100: 12253-12258.
16. Feltus FA, Lee EK, Costello JF, Plass C, Vertino PM. 2006. DNA motifs associated with aberrant CpG island methylation. Genomics 87: 572-579.
17. Ganapathi M, Srivastava P, Das Sutar SK, Kumar K, Dasgupta D, Pal Singh G, Brahmachari V, Brahmachari SK. 2005. Comparative analysis of chromatin landscape in regulatory regions of human housekeeping and tissue specific genes. BMC Bioinformatics 6: 126. doi: 10.1186/1471-2105-6-126.
18. Gardiner-Garden M, Frommer M. 1987. CpG islands in vertebrate genomes. J Mol Biol 196: 261-282.
19. Gdula DA, Gerasimova TI, Corces VG. 1996. Genetic and molecular analysis of the gypsy chromatin insulator of Drosophila. Proc Natl Acad Sci 93: 9378-9383.
20. Greally JM. 2002. Short interspersed transposable elements (SINEs) are excluded from imprinted regions in the human genome. Proc Natl Acad Sci 99: 327-332.
21. Hahn MA, Hahn T, Lee DH, Esworthy RS, Kim BW, Riggs AD, Chu FF, Pfeifer GP. 2008. Methylation of polycomb target genes in intestinal cancer is mediated by inflammation. Cancer Res 68: 10280-10289.
22. Han JS, Szak ST, Boeke JD. 2004. Transcriptional disruption by the L1 retrotransposon and implications for mammalian transcriptomes. Nature 429: 268-274.
23. Hollister JD, Gaut BS. 2009. Epigenetic silencing of transposable elements: A trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res 19: 1419-1428.
24. Jones PA, Baylin SB. 2002. The fundamental role of epigenetic events in cancer. Natl Rev 3: 415-428.
25. Jurka J, Kohany O, Pavlicek A, Kapitonov VV, Jurka MV. 2004. Duplication, coclustering, and selection of human Alu retrotransposons. Proc Natl Acad Sci 101: 1268-1272.
26. Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, Haussler D, Kent WJ. 2004. The UCSC Table Browser data retrieval tool. Nucleic Acids Res 32: D493-D496.
27. Kondo E, Furukawa T, Yoshinaga K, Kijima H, Semba S, Yatsuoka T, Yokoyama T, Fukushige S, Horii A. 2000. Not hMSH2 but hMLH1 is frequently silenced by hypermethylation in endometrial cancer but rarely silenced in pancreatic cancer with microsatellite instability. Int J Oncol 17: 535-541.
28. Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C, Yamochi T, Urano T, Furukawa K, Kwabi-Addo B, et al. 2008. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet 40: 741-750.
29. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, et al. 2006. Control of developmental regulators by Polycomb inhuman embryonic stem cells. Cell 125: 301-313.
30. Lin YW, Slape C, Zhang Z, Aplan PD. 2005. NUP98-HOXD13 transgenic mice develop a highly penetrant, severe myelodysplastic syndrome that progresses to acute leukemia. Blood 106: 287-295.
31. Lunyak VV, Prefontaine GG, Núñez E, Cramer T, Ju BG, Ohgi KA, Hutt K, Roy R, García-Díaz A, Zhu X, et al. 2007. Developmentally regulated activation of a SINE B2 repeat as a domain boundary in organogenesis. Science 317: 248-251.
32. McCabe MT, Lee EK, Vertino PM. 2009. A multifactorial signature of DNA sequence and polycomb binding predicts aberrant CpG island methylation. Cancer Res 69: 282-291.
33. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, et al. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560.
34. Mouse Genome Sequencing Consortium. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562.
35. Mummaneni P, Yates P, Simpson J, Rose J, Turker MS. 1998. The primary function of a redundant Sp1 binding site in themouse aprt gene promoter is to block epigenetic gene inactivation. Nucleic Acids Res 26: 5163-5169. (Pubitemid 28517574)
36. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, Mohammad HP, Chen W, Daniel VC, Yu W, 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.
37. Ross DT, Scherf U, Eisen MB, Perou CM, Rees C, Spellman P, Iyer V, Jeffrey SS, Van de Rijn M, Waltham M, et al. 2000. Systematic variation in gene expression patterns in human cancer cell lines. Nat Genet 24: 227-235.
38. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, Eden E, Yakhini Z, Ben-Shushan E, Reubinoff BE, 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.
39. Shen L, Kondo Y, Ahmed S, Boumber Y, Konishi K, Guo Y, Chen X, Vilaythong JN, Issa JP. 2007a. Drug sensitivity prediction by CpG island methylation profile in the NCI-60 cancer cell line panel. Cancer Res 67: 11335-11343.
40. Shen L, Kondo Y, Guo Y, Zhang J, Zhang L, Ahmed S, Shu J, Chen X, Waterland RA, Issa JP. 2007b. Genome-wide profiling of DNA methylation reveals a class of normally methylated CpG island promoters. PLoS Genet 3: e181. doi: 10.1371/journal.pgen.0030181.
41. Simons C, Pheasant M, Makunin IV, Mattick JS. 2006. Transposon-free regions in mammalian genomes. Genome Res 16: 164-172.
42. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, et al. 2004. A gene atlas of themouse and human protein-encoding transcriptomes. Proc Natl Acad Sci 101: 6062-6067.
43. Takai D, Jones PA. 2003. The CpG island searcher: A new WWW resource. In Silico Biol 3: 235-240.
44. Tanay A, O'Donnell AH, Damelin M, Bestor TH. 2007. Hyperconserved CpG domains underlie Polycomb-binding sites. Proc Natl Acad Sci 104: 5521-5526.
45. Toyota M, Issa JP. 1999. CpG island methylator phenotypes in aging and cancer. Semin Cancer Biol 9: 349-357. (Pubitemid 29532861)
46. Wang Z, Willard HF, Mukherjee S, Furey TS. 2006. Evidence of influence of genomic DNA sequence on human X chromosome inactivation. PLoS Comput Biol 2: e113. doi: 10.1371/journal.pcbi.0020113.
47. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, Rebhan M, Schubeler D. 2007. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39: 457-466.
48. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C, Weisenberger DJ, Campan M, Young J, Jacobs I, et al. 2007. Epigenetic stem cell signature in cancer. Nat Genet 39: 157-158.
49. Yates PA, Burman RW, Mummaneni P, Krussel S, Turker MS. 1999. Tandem B1 elements located in a mouse methylation center provide a target for de novo DNA methylation. J Biol Chem 274: 36357-36361.
50. Yoder JA, Walsh CP, Bestor TH. 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13: 335-340.