DNA methylome analysis in Burkitt and follicular lymphomas identifies differentially methylated regions linked to somatic mutation and transcriptional control

Nature Genetics

Volumn 47, Issue 11, 2015, Pages 1316-1325

  Kretzmer, Helene ^a   Bernhart, Stephan H ^a   Wang, Wei ^b   Haake, Andrea ^c   Weniger, Marc A ^d   Bergmann, Anke K ^c,e   Betts, Matthew J ^f   Carrillo de Santa Pau, Enrique ^g   Doose, Gero ^a   Gutwein, Jana ^c   Richter, Julia ^c   Hovestadt, Volker ^b   Huang, Bingding ^b   Rico, Daniel ^g   Jühling, Frank ^a   Kolarova, Julia ^c   Lu, Qianhao ^f   Otto, Christian ^a   Wagener, Rabea ^c   Arnolds, Judith ^d   Burkhardt, Birgit ^h   Claviez, Alexander ^e   Drexler, Hans G ⁱ   Eberth, Sonja ^i,j   Eils, Roland ^b,f   Flicek, Paul ^k   Haas, Siegfried ^l   Hummel, Michael ^m   Karsch, Dennis ^e   Kerstens, Hinrik H D ⁿ   Klapper, Wolfram ^c   Kreuz, Markus ^a   Lawerenz, Chris ^b   Lenze, Dido ^m   Loeffler, Markus ^a   López, Cristina ^c   MacLeod, Roderick A F ⁱ   Martens, Joost H A ⁿ   Kulis, Marta ⁿ   Martín Subero, José Ignacio ^o   Möller, Peter ^p   Nagel, Inga ^c   Picelli, Simone ^b   Vater, Inga ^c   Rohde, Marius ^q   Rosenstiel, Philip ^c   Rosolowski, Maciej ^a   Russell, Robert B ^f   Schilhabel, Markus ^c   Schlesner, Matthias ^b   Stadler, Peter F ^a,r,s,t   Szczepanowski, Monika ⁿ   Trümper, Lorenz ^j   Stunnenberg, Hendrik G ⁿ   Küppers, Ralf ^d   Ammerpohl, Ole ^c   Lichter, Peter ^b   Siebert, Reiner ^c   Hoffmann, Steve ^a   Radlwimmer, Bernhard ^b   more..

^a UNIVERSITY OF LEIPZIG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF KIEL   (Germany)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

^e UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^f UNIVERSITY OF HEIDELBERG   (Germany)

^g Structural Biology and Biocomputing Programme   (Spain)

^h UNIVERSITY HOSPITAL MÜNSTER   (Germany)

ⁱ LEIBNIZ INSTITUTE DSMZ GERMAN COLLECTION OF MICROORGANISMS AND CELL CULTURES   (Germany)

^j UNIVERSITY OF GÖTTINGEN   (Germany)

^k WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^l Friedrich Ebert Krankenhaus   (Germany)

^m CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

ⁿ RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^o UNIVERSITY OF BARCELONA   (Spain)

^p UNIVERSITY OF ULM MEDICAL SCHOOL   (Germany)

^q UNIVERSITY HOSPITAL GIESSEN   (Germany)

^r FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

^s SANTA FE INSTITUTE   (United States)

^t MAX PLANCK INSTITUTE FOR MATHEMATICS IN THE SCIENCES   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE; BMI1 PROTEIN; BRG1 PROTEIN; INHIBITOR OF DIFFERENTIATION 3; MYC PROTEIN; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN BCL 3; PROTEIN SWI; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR 2; STAT5A PROTEIN; TRANSCRIPTION FACTOR 7 LIKE 1; TRANSCRIPTION FACTOR SNF; TRANSCRIPTION FACTOR YY1; TRANSCRIPTION FACTOR ZEB1; TRANSCRIPTOME; UNCLASSIFIED DRUG; MYC PROTEIN, HUMAN; ONCOPROTEIN; PROTEIN BCL 2;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; BURKITT LYMPHOMA; CARBOXY TERMINAL SEQUENCE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; FOLLICULAR LYMPHOMA; GENE EXPRESSION; GENE SEQUENCE; GERMINAL CENTER; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; NONSENSE MUTATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; SOMATIC MUTATION; TRANSCRIPTION REGULATION; UPREGULATION; ADOLESCENT; ADULT; AGED; B LYMPHOCYTE; CHILD; FEMALE; GENE TRANSLOCATION; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN GENOME; MALE; METABOLISM; MIDDLE AGED; MUTATION; PRESCHOOL CHILD; PROCEDURES; TUMOR CELL LINE; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; B-LYMPHOCYTES; BURKITT LYMPHOMA; CELL LINE, TUMOR; CHILD; CHILD, PRESCHOOL; DNA METHYLATION; FEMALE; GENOME, HUMAN; GERMINAL CENTER; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LYMPHOMA, FOLLICULAR; MALE; MIDDLE AGED; MUTATION; ONCOGENE PROTEINS, FUSION; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-MYC; SIGNAL TRANSDUCTION; TRANSCRIPTOME; TRANSLOCATION, GENETIC; YOUNG ADULT;

EID: 84995360059     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3413     Document Type: Article

References (55)

1. Lai, A.Y., et al. DNA methylation profiling in human B cells reveals immune regulatory elements and epigenetic plasticity at Alu elements during B-cell activation. Genome Res. 23, 2030-2041 (2013).
2. Lee, S.T., et al. A global DNA methylation and gene expression analysis of early human B-cell development reveals a demethylation signature and transcription factor network. Nucleic Acids Res. 40, 11339-11351 (2012).
3. Shaknovich, R., et al. DNA methyltransferase 1 and DNA methylation patterning contribute to germinal center B-cell differentiation. Blood 118, 3559-3569 (2011).
4. Basso, K., & Dalla-Favera, R. Germinal centres and B cell lymphomagenesis. Nat. Rev. Immunol. 15, 172-184 (2015).
5. Lenz, G., & Staudt, L.M. Aggressive lymphomas. N. Engl. J. Med. 362, 1417-1429 (2010).
6. Küppers, R., & Dalla-Favera, R. Mechanisms of chromosomal translocations in B cell lymphomas. Oncogene 20, 5580-5594 (2001).
7. Dave, S.S., et al. Molecular diagnosis of Burkitt's lymphoma. N. Engl. J. Med. 354, 2431-2442 (2006).
8. Richter, J., et al. Recurrent mutation of the ID3 gene in Burkitt lymphoma identified by integrated genome, exome and transcriptome sequencing. Nat. Genet. 44, 1316-1320 (2012).
9. Schmitz, R., et al. Burkitt lymphoma pathogenesis and therapeutic targets from structural and functional genomics. Nature 490, 116-120 (2012).
10. Loeffler, M., et al. Genomic and epigenomic co-evolution in follicular lymphomas. Leukemia 29, 456-463 (2015).
11. Morin, R.D., et al. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat. Genet. 42, 181-185 (2010).
12. Morin, R.D., et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature 476, 298-303 (2011).
13. Okosun, J., et al. Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat. Genet. 46, 176-181 (2014).
14. Pasqualucci, L., et al. Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature 471, 189-195 (2011).
15. Victora, G.D., et al. Identification of human germinal center light and dark zone cells and their relationship to human B-cell lymphomas. Blood 120, 2240-2248 (2012).
16. Otto, C., Stadler, P.F., & Hoffmann, S. Fast and sensitive mapping of bisulfite-Dreated sequencing data. Bioinformatics 28, 1698-1704 (2012).
17. Ernst, J., et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43-49 (2011).
18. Hahn, M.A., et al. Loss of the Polycomb mark from bivalent promoters leads to activation of cancer-promoting genes in colorectal tumors. Cancer Res. 74, 3617-3629 (2014).
19. Hovestadt, V., et al. Decoding the regulatory landscape of medulloblastoma using DNA methylation sequencing. Nature 510, 537-541 (2014).
20. Weidensdorfer, D., et al. Control of c-myc mRNA stability by IGF2BP1-Associated cytoplasmic RNPs. RNA 15, 104-115 (2009).
21. Hummel, M., et al. A biologic definition of Burkitt's lymphoma from transcriptional and genomic profiling. N. Engl. J. Med. 354, 2419-2430 (2006).
22. Love, C., et al. The genetic landscape of mutations in Burkitt lymphoma. Nat. Genet. 44, 1321-1325 (2012).
23. Muppidi, J.R., et al. Loss of signalling via Galpha13 in germinal centre B-cell-derived lymphoma. Nature 516, 254-258 (2014).
24. Rohde, M., et al. Recurrent RHOA mutations in pediatric Burkitt lymphoma treated according to the NHL-BFM protocols. Genes Chromosom. Cancer 53, 911-916 (2014).
25. O'Hayre, M., et al. The emerging mutational landscape of G proteins and G-protein-coupled receptors in cancer. Nat. Rev. Cancer 13, 412-424 (2013).
26. Takuwa, N., et al. Tumor-suppressive sphingosine-1-phosphate receptor-2 counteracting tumor-promoting sphingosine-1-phosphate receptor-1 and sphingosine kinase 1-Jekyll hidden behind Hyde. Am. J. Cancer Res. 1, 460-481 (2011).
27. Morin, R.D., et al. Mutational and structural analysis of diffuse large B-cell lymphoma using whole-genome sequencing. Blood 122, 1256-1265 (2013).
28. Abraham, B.J., Cui, K., Tang, Q., & Zhao, K. Dynamic regulation of epigenomic landscapes during hematopoiesis. BMC Genomics 14, 193 (2013).
29. Scott, C.L., et al. Role of the chromobox protein CBX7 in lymphomagenesis. Proc. Natl. Acad. Sci. USA 104, 5389-5394 (2007).
30. Dykhuizen, E.C., et al. BAF complexes facilitate decatenation of DNA by topoisomerase IIa. Nature 497, 624-627 (2013).
31. Klapper, W., et al. Patient age at diagnosis is associated with the molecular characteristics of diffuse large B-cell lymphoma. Blood 119, 1882-1887 (2012).
32. Hasselblatt, M., et al. Nonsense mutation and inactivation of SMARCA4 (BRG1) in an atypical teratoid/rhabdoid tumor showing retained SMARCB1 (INI1) expression. Am. J. Surg. Pathol. 35, 933-935 (2011).
33. Hasselblatt, M., et al. SMARCA4-mutated atypical teratoid/rhabdoid tumors are associated with inherited germline alterations and poor prognosis. Acta Neuropathol. 128, 453-456 (2014).
34. Schneppenheim, R., et al. Germline nonsense mutation and somatic inactivation of SMARCA4/BRG1 in a family with rhabdoid tumor predisposition syndrome. Am. J. Hum. Genet. 86, 279-284 (2010).
35. Witkowski, L., et al. Germline and somatic SMARCA4 mutations characterize small cell carcinoma of the ovary, hypercalcemic type. Nat. Genet. 46, 438-443 (2014).
36. Betts, M.J., et al. Mechismo: predicting the mechanistic impact of mutations and modifications on molecular interactions. Nucleic Acids Res. 43, e10 (2015).
37. Kulis, M., et al. Whole-genome fingerprint of the DNA methylome during human B cell differentiation. Nat. Genet. 47, 746-756 (2015).
38. Lister, R., et al. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471, 68-73 (2011).
39. Bibikova, M., et al. High density DNA methylation array with single CpG site resolution. Genomics 98, 288-295 (2011).
40. Li, H., & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
41. Jones, D.T., et al. Recurrent somatic alterations of FGFR1 and NTRK2 in pilocytic astrocytoma. Nat. Genet. 45, 927-932 (2013).
42. Rimmer, A., et al. Integrating mapping-, assembly-And haplotype-based approaches for calling variants in clinical sequencing applications. Nat. Genet. 46, 912-918 (2014).
43. Hoffmann, S., et al. Fast mapping of short sequences with mismatches, insertions and deletions using index structures. PLoS Comput. Biol. 5, e1000502 (2009).
44. Zhang, N.R., & David, O.S. Model selection for high-dimensional, multisequence change-point problems. Stat. Sin. 22, 1507 (2012).
45. Anders, S., & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
46. Karolchik, D., et al. The UCSC Genome Browser database: 2014 update. Nucleic Acids Res. 42, D764-D770 (2014).
47. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
48. Flicek, P., et al. Ensembl 2014. Nucleic Acids Res. 42, D749-D755 (2014).
49. Ernst, J., & Kellis, M. ChromHMM: automating chromatin-state discovery and characterization. Nat. Methods 9, 215-216 (2012).
50. Dürr, H., et al. X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 121, 363-373 (2005).
51. Eswar, N., et al. Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics 47, 5.6.1-5.6.32 (2006).
52. Sharma, V., et al. Crystal structure of Mycobacterium tuberculosis SecA, a preprotein translocating ATPase. Proc. Natl. Acad. Sci. USA 100, 2243-2248 (2003).
53. Huber, W., et al. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18, S96-S104 (2002).
54. Bentink, S., et al. Pathway activation patterns in diffuse large B-cell lymphomas. Leukemia 22, 1746-1754 (2008).
55. Wright, G., et al. A gene expression-based method to diagnose clinically distinct subgroups of diffuse large B cell lymphoma. Proc. Natl. Acad. Sci. USA 100, 9991-9996 (2003).