Nanoscale chromatin profiling of gastric adenocarcinoma reveals cancer-associated cryptic promoters and somatically acquired regulatory elements

Nature Communications

Volumn 5, Issue , 2014, Pages

  Muratani, Masafumi ^a,i   Deng, Niantao ^b,c   Ooi, Wen Fong ^a   Lin, Suling Joyce ^a   Xing, Manjie ^b,c   Xu, Chang ^d   Qamra, Aditi ^a,e   Tay, Su Ting ^b,f   Malik, Simeen ^b   Wu, Jeanie ^f   Lee, Ming Hui ^f   Zhang, Shenli ^b   Tan, Luke Lin Chuen ^b   Chua, Huihoon ^a   Wong, Wai Keong ^g   Ong, Hock Soo ^g   Ooi, London Lucien ^g   Chow, Pierce Kah How ^b,g,h   Chan, Weng Hoong ^g   Soo, Khee Chee ^h   Goh, Liang Kee ^b   Rozen, Steve ^b   Teh, Bin Tean ^b,d,h   Yu, Qiang ^a   Ng, Huck Hui ^a   Tan, Patrick ^a,b,d,f   more..

^a GENOME INSTITUTE OF SINGAPORE   (Singapore)

^b DUKE NUS MEDICAL SCHOOL   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^f INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^g SINGAPORE GENERAL HOSPITAL   (Singapore)

^h DIVISION OF MEDICAL ONCOLOGY   (Singapore)

ⁱ UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; POLYCOMB REPRESSIVE COMPLEX 2; CHROMATIN; DNA; HISTONE;

CANCER; CHROMOSOME; DIGESTIVE SYSTEM DISORDER; GENE EXPRESSION; GENETIC VARIATION; MUTATION;

ARTICLE; CANCER DIAGNOSIS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CRYPTIC PROMOTER; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE MARKER; DNA METHYLATION; ENHANCER REGION; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HISTONE MODIFICATION; HUMAN; HUMAN TISSUE; INTESTINE METAPLASIA; MAJOR CLINICAL STUDY; NANOCHIP; PROMOTER REGION; REGULATORY SEQUENCE; SENSITIVITY AND SPECIFICITY; SINGLE NUCLEOTIDE POLYMORPHISM; SOLID TUMOR; SOMATIC MUTATION; STOMACH ADENOCARCINOMA; TRANSCRIPTION INITIATION SITE; ADENOCARCINOMA; ALLELE; CASE CONTROL STUDY; CHROMATIN; DNA FINGERPRINTING; GENETICS; MUTATION; NANOTECHNOLOGY; PATHOLOGY; PROCEDURES; STOMACH TUMOR;

ADENOCARCINOMA; ALLELES; CASE-CONTROL STUDIES; CHROMATIN; DNA; DNA FINGERPRINTING; DNA METHYLATION; DNA, NEOPLASM; HISTONES; HUMANS; MUTATION; NANOTECHNOLOGY; PROMOTER REGIONS, GENETIC; REGULATORY ELEMENTS, TRANSCRIPTIONAL; STOMACH NEOPLASMS; TRANSCRIPTION INITIATION SITE;

EID: 84904310622     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5361     Document Type: Article

References (70)

1. Ferlay, J. et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer 127, 2893-2917 (2010).
2. Wang, K. et al. Exome sequencing identifies frequent mutation of ARID1A in molecular subtypes of gastric cancer. Nat. Genet. 43, 1219-1223 (2011).
3. Nagarajan, N. et al. Whole-genome reconstruction and mutational signatures in gastric cancer. Genome Biol. 13, R115 (2012).
4. Zang, Z. J. et al. Exome sequencing of gastric adenocarcinoma identifies recurrent somatic mutations in cell adhesion and chromatin remodeling genes. Nat. Genet. 44, 570-574 (2012).
5. Visel, A. et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858 (2009).
6. Akhtar-Zaidi, B. et al. Epigenomic enhancer profiling defines a signature of colon cancer. Science 336, 736-739 (2012).
7. Zhu, J. et al. Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152, 642-654 (2013).
8. Nguyen, C. T., Gonzales, F. A. & Jones, P. A. Altered chromatin structure associated with methylation-induced gene silencing in cancer cells: correlation of accessibility, methylation, MeCP2 binding and acetylation. Nucleic Acids Res. 29, 4598-4606 (2001). (Pubitemid 33095020)
9. Black, J. C. et al. KDM4A lysine demethylase induces site-specific copy gain and rereplication of regions amplified in tumours. Cell 154, 541-555 (2013).
10. Esteller, M. & Herman, J. G. Cancer as an epigenetic disease: DNA methylation and chromatin alterations in human tumours. J. Pathol. 196, 1-7 (2002).
11. Ushijima, T. & Hattori, N. Molecular pathways: involvement of Helicobacter pylori-triggered inflammation in the formation of an epigenetic field defect, and its usefulness as cancer risk and exposure markers. Clin. Cancer Res. 18, 923-929 (2012).
12. Machado, J. C. et al. E-cadherin gene (CDH1) promoter methylation as the second hit in sporadic diffuse gastric carcinoma. Oncogene 20, 1525-1528 (2001).
13. Homma, N. et al. Spreading of methylation within RUNX3 CpG island in gastric cancer. Cancer Sci. 97, 51-56 (2006). (Pubitemid 43257027)
14. Ivanova, T. et al. Integrated epigenomics identifies BMP4 as a modulator of cisplatin sensitivity in gastric cancer. Gut 62, 22-33 (2013).
15. Sugita, H. et al. Methylation of BNIP3 and DAPK indicates lower response to chemotherapy and poor prognosis in gastric cancer. Oncol. Rep. 25, 513-518 (2011).
16. Li, X. et al. Epigenetic inactivation of paired box gene 5, a novel tumour suppressor gene, through direct upregulation of p53 is associated with prognosis in gastric cancer patients. Oncogene 31, 3419-3430 (2012).
17. Shin, C. M. et al. Genome-wide DNA methylation profiles in noncancerous gastric mucosae with regard to Helicobacter pylori infection and the presence of gastric cancer. Helicobacter 16, 179-188 (2011).
18. Zouridis, H. et al. Methylation subtypes and large-scale epigenetic alterations in gastric cancer. Sci. Transl. Med. 4, 156ra140 (2012).
19. Matsusaka, K. et al. Classification of Epstein-Barr virus-positive gastric cancers by definition of DNA methylation epigenotypes. Cancer Res. 71, 7187-7197 (2011).
20. Zhang, L., Zhong, K., Dai, Y. & Zhou, H. Genome-wide analysis of histone H3 lysine 27 trimethylation by ChIP-chip in gastric cancer patients. J. Gastroenterol. 44, 305-312 (2009).
21. Smiraglia, D. J. et al. Excessive CpG island hypermethylation in cancer cell lines versus primary human malignancies. Hum. Mol. Genet. 10, 1413-1419 (2001). (Pubitemid 32640670)
22. Tanasijevic, B. et al. Progressive accumulation of epigenetic heterogeneity during human ES cell culture. Epigenetics 4, 330-338 (2009).
23. Ng, J. H. et al. In vivo epigenomic profiling of germ cells reveals germ cell molecular signatures. Dev. Cell 24, 324-333 (2013).
24. Wang, Z. et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40, 897-903 (2008). (Pubitemid 351913645)
25. Rada-Iglesias, A. et al. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470, 279-283 (2011).
26. Creyghton, M. P. et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl Acad. Sci. USA 107, 21931-21936 (2010).
27. Xu, H. et al. A signal-noise model for significance analysis of ChIP-seq with negative control. Bioinformatics 26, 1199-1204 (2010).
28. Deng, N. et al. A comprehensive survey of genomic alterations in gastric cancer reveals systematic patterns of molecular exclusivity and co-occurrence among distinct therapeutic targets. Gut 61, 673-684 (2012).
29. Barros, R., Freund, J. N., David, L. & Almeida, R. Gastric intestinal metaplasia revisited: function and regulation of CDX2. Trends Mol. Med. 18, 555-563 (2012).
30. Ernst, J. et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43-49 (2011).
31. Wamstad, J. A. et al. Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell 151, 206-220 (2012).
32. Bernstein, B. E. et al. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
33. Thurman, R. E. et al. The accessible chromatin landscape of the human genome. Nature 489, 75-82 (2012).
34. McLean, C. Y. et al. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501 (2010).
35. Kong-Beltran, M., Stamos, J. & Wickramasinghe, D. The Sema domain of Met is necessary for receptor dimerization and activation. Cancer Cell 6, 75-84 (2004). (Pubitemid 38903163)
36. Hafler, B. P., Choi, M. Y., Shivdasani, R. A. & Rowitch, D. H. Expression and function of Nkx6.3 in vertebrate hindbrain. Brain Res. 1222, 42-50 (2008).
37. Choi, M. Y. et al. Requirement of the tissue-restricted homeodomain transcription factor Nkx6.3 in differentiation of gastrin-producing G cells in the stomach antrum. Mol. Cell. Biol. 28, 3208-3218 (2008). (Pubitemid 351657086)
38. Hayashida, T. et al. HOXB9, a gene overexpressed in breast cancer, promotes tumorigenicity and lung metastasis. Proc. Natl Acad. Sci. USA 107, 1100-1105 (2010).
39. Wang, J. et al. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 22, 1798-1812 (2012).
40. Lee, T. I. et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125, 301-313 (2006). (Pubitemid 44313811)
41. Margueron, R. & Reinberg, D. The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349 (2011).
42. Ku, M. et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4, e1000242 (2008).
43. Bernstein, B. E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326 (2006).
44. Ohm, J. E. et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat. Genet. 39, 237-242 (2007). (Pubitemid 46184356)
45. Cibulskis, K. et al. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat. Biotechnol. 31, 213-219 (2013).
46. Abecasis, G. R. et al. An integrated map of genetic variation from 1, 092 human genomes. Nature 491, 56-65 (2012).
47. Kilpinen, H. et al. Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription. Science 342, 744-747 (2013).
48. Kasowski, M. et al. Extensive variation in chromatin states across humans. Science 342, 750-752 (2013).
49. Boyle, A. P. et al. Annotation of functional variation in personal genomes using RegulomeDB. Genome Res. 22, 1790-1797 (2012).
50. Kwon, M. J. et al. Claudin-4 overexpression is associated with epigenetic derepression in gastric carcinoma. Lab. Invest. 91, 1652-1667 (2011).
51. Powell, E. L. et al. Concordant loss of MTAP and p16/CDKN2A expression in gastroesophageal carcinogenesis: evidence of homozygous deletion in esophageal noninvasive precursor lesions and therapeutic implications. Am. J. Surg. Pathol. 29, 1497-1504 (2005). (Pubitemid 41513300)
52. Lei, K. F. et al. SerpinB5 interacts with KHDRBS3 and FBXO32 in gastric cancer cells. Oncol. Rep. 26, 1115-1120 (2011).
53. Li, Z. et al. Up-regulation of a HOXA-PBX3 homeobox-gene signature following down-regulation of miR-181 is associated with adverse prognosis in patients with cytogenetically abnormal AML. Blood 119, 2314-2324 (2012).
54. Selamat, S. A. et al. DNA methylation changes in atypical adenomatous hyperplasia, adenocarcinoma in situ, and lung adenocarcinoma. PLoS ONE 6, e21443 (2011).
55. Tsunoda, T. & Takagi, T. Estimating transcription factor bindability on DNA. Bioinformatics 15, 622-630 (1999). (Pubitemid 29462111)
56. Vernot, B. et al. Personal and population genomics of human regulatory variation. Genome Res. 22, 1689-1697 (2012).
57. Greer, E. L. & Shi, Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nat. Rev. Genet. 13, 343-357 (2012).
58. Jakovcevski, M. & Akbarian, S. Epigenetic mechanisms in neurological disease. Nat. Med. 18, 1194-1204 (2012).
59. Huang, F. W. et al. Highly recurrent TERT promoter mutations in human melanoma. Science 339, 957-959 (2013).
60. Horn, S. et al. TERT promoter mutations in familial and sporadic melanoma. Science 339, 959-961 (2013).
61. Birney, E. et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447, 799-816 (2007). (Pubitemid 46920138)
62. Network, C. G. A. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337 (2012).
63. Schuster-Böckler, B. & Lehner, B. Chromatin organization is a major influence on regional mutation rates in human cancer cells. Nature 488, 504-507 (2012).
64. Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515 (2010).
65. Johnson, W. E., Li, C. & Rabinovic, A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics. 8, 118-127 (2007). (Pubitemid 44906106)
66. Harrow, J. et al. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 22, 1760-1774 (2012).
67. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).
68. Teschendorff, A. E. et al. A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinformatics 29, 189-196 (2013).
69. McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010).
70. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 25, 2078-2079 (2009).