Genetic and epigenetic profiling of CLL disease progression reveals limited somatic evolution and suggests a relationship to memory-cell development

Blood Cancer Journal

Volumn 5, Issue 4, 2015, Pages

  Smith, E N ^a,b   Ghia, E M ^b,c   Deboever, C M ^c   Rassenti, L Z ^b,c   Jepsen, K ^c   Yoon, K A ^a   Matsui, H ^a,c   Rozenzhak, S ^a,b   Alakus, H ^a,b   Shepard, P J ^a,b   Dai, Y ^a,b   Khosroheidari, M ^c   Bina, M ^d   Gunderson, K L ^e   Messer, K ^b   Muthuswamy, L ^f,g   Hudson, T J ^f,g   Harismendy, O ^a,b   Barrett, C L ^a,b   Jamieson, C H M ^b,c   Carson, D A ^b,c   Kipps, T J ^b,c   Frazer, K A ^a,b,c   more..

^a RADY CHILDREN'S HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d PURDUE UNIVERSITY   (United States)

^e ILLUMINA INC   (United States)

^f ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

^g UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCOMB GROUP PROTEIN;

CHRONIC LYMPHATIC LEUKEMIA; CLONAL EVOLUTION; CPG ISLAND; DISEASE COURSE; DNA METHYLATION; GENETIC EPIGENESIS; GENETICS; HUMAN; MUTATION; PATHOLOGY;

CLONAL EVOLUTION; CPG ISLANDS; DISEASE PROGRESSION; DNA METHYLATION; EPIGENESIS, GENETIC; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MUTATION; POLYCOMB-GROUP PROTEINS;

EID: 84961551939     PISSN: None     EISSN: 20445385     Source Type: Journal    
DOI: 10.1038/BCJ.2015.14     Document Type: Article

References (39)

1. Greaves M, Maley CC. Clonal evolution in cancer. Nature 2012; 481: 306–313.
2. Hallek M, Cheson BD, Catovsky D, Caligaris-Cappio F, Dighiero G, Dohner H et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute-Working Group 1996 guidelines. Blood 2008; 111: 5446–5456.
3. Landau DA, Carter SL, Stojanov P, McKenna A, Stevenson K, Lawrence MS et al. Evolution and impact of subclonal mutations in chronic lymphocytic leukemia. Cell 2013; 152: 714–726.
4. Burrell RA, McGranahan N, Bartek J, Swanton C. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 2013; 501: 338–345.
5. Ojha J, Ayres J, Secreto C, Tschumper R, Rabe K, Van Dyke D et al. Deep sequencing identifies genetic heterogeneity and recurrent convergent evolution in chronic lymphocytic leukemia. Blood 2015; 125: 492–498.
6. Braggio E, Kay NE, VanWier S, Tschumper RC, Smoley S, Eckel-Passow JE et al. Longitudinal genome-wide analysis of patients with chronic lymphocytic leukemia reveals complex evolution of clonal architecture at disease progression and at the time of relapse. Leukemia 2012; 26: 1698–1701.
7. Timp W, Feinberg AP. Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host. Nat Rev Cancer 2013; 13: 497–510.
8. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 2007; 39: 232–236.
9. Mack SC, Witt H, Piro RM, Gu L, Zuyderduyn S, Stutz AM et al. Epigenomic alterations define lethal CIMP-positive ependymomas of infancy. Nature 2014; 506: 445–450.
10. 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.
11. Cahill N, Bergh AC, Kanduri M, Goransson-Kultima H, Mansouri L, Isaksson A et al. 450K-array analysis of chronic lymphocytic leukemia cells reveals global DNA methylation to be relatively stable over time and similar in resting and pro-liferative compartments. Leukemia 2013; 27: 150–158.
12. Tewhey R, Nakano M, Wang X, Pabon-Pena C, Novak B, Giuffre A et al. Enrichment of sequencing targets from the human genome by solution hybridization. Genome Biol 2009; 10: R116.
13. Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 2010; 26: 589–595.
14. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 2011; 43: 491–498.
15. Smith EN, Jepsen K, Khosroheidari M, Rassenti LZ, M DA, Ghia EM et al. Biased estimates of clonal evolution and subclonal heterogeneity can arise from PCR duplicates in deep sequencing experiments. Genome Biol 2014; 15: 420.
16. Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics 2012; 13: 86.
17. Calvanese V, Fernandez AF, Urdinguio RG, Suarez-Alvarez B, Mangas C, Perez-Garcia V et al. A promoter DNA demethylation landscape of human hematopoietic differentiation. Nucleic Acids Res 2012; 40: 116–131.
18. Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 2010; 11: R14.
19. Geeleher P, Hartnett L, Egan LJ, Golden A, Raja Ali RA, Seoighe C. Gene-set analysis is severely biased when applied to genome-wide methylation data. Bioinformatics 2013; 29: 1851–1857.
20. Velichutina I, Shaknovich R, Geng H, Johnson NA, Gascoyne RD, Melnick AM et al. EZH2-mediated epigenetic silencing in germinal center B cells contributes to proliferation and lymphomagenesis. Blood 2010; 116: 5247–5255.
21. Chen SS, Raval A, Johnson AJ, Hertlein E, Liu TH, Jin VX et al. Epigenetic changes during disease progression in a murine model of human chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2009; 106: 13433–13438.
22. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol 2013; 14: R115.
23. Teschendorff AE, Menon U, Gentry-Maharaj A, Ramus SJ, Weisenberger DJ, Shen H et al. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res 2010; 20: 440–446.
24. Weidner CI, Lin Q, Koch CM, Eisele L, Beier F, Ziegler P et al. Aging of blood can be tracked by DNA methylation changes at just three CpG sites. Genome Biol 2014; 15: R24.
25. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26: 841–842.
26. Dohner H, Stilgenbauer S, Benner A, Leupolt E, Krober A, Bullinger L et al. Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med 2000; 343: 1910–1916.
27. Rassenti LZ, Huynh L, Toy TL, Chen L, Keating MJ, Gribben JG et al. ZAP-70 compared with immunoglobulin heavy-chain gene mutation status as a predictor of disease progression in chronic lymphocytic leukemia. N Engl J Med 2004; 351: 893–901.
28. Roth A, Khattra J, Yap D, Wan A, Laks E, Biele J et al. PyClone: statistical inference of clonal population structure in cancer. Nat Methods 2014; 11: 396–398.
29. Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, Mikkelsen TS et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 2008; 4: e1000242.
30. Raney BJ, Cline MS, Rosenbloom KR, Dreszer TR, Learned K, Barber GP et al. ENCODE whole-genome data in the UCSC genome browser (2011 update). Nucleic Acids Res 2011; 39: D871–D875.
31. Raval A, Tanner SM, Byrd JC, Angerman EB, Perko JD, Chen SS et al. Downregulation of death-associated protein kinase 1 (DAPK1) in chronic lymphocytic leukemia. Cell 2007; 129: 879–890.
32. Seeliger B, Wilop S, Osieka R, Galm O, Jost E. CpG island methylation patterns in chronic lymphocytic leukemia. Leuk Lymphoma 2009; 50: 419–426.
33. Claus R, Lucas DM, Ruppert AS, Williams KE, Weng D, Patterson K et al. Validation of ZAP-70 methylation and its relative significance in predicting outcome in chronic lymphocytic leukemia. Blood 2014; 124: 42–48.
34. Kulis M, Heath S, Bibikova M, Queiros AC, Navarro A, Clot G et al. Epigenomic analysis detects widespread gene-body DNA hypomethylation in chronic lymphocytic leukemia. Nat Genet 2012; 44: 1236–1242.
35. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C et al. Epigenetic stem cell signature in cancer. Nat Genet 2007; 39: 157–158.
36. Fegan C, Robinson H, Thompson P, Whittaker JA, White D. Karyotypic evolution in CLL: identification of a new sub-group of patients with deletions of 11q and advanced or progressive disease. Leukemia 1995; 9: 2003–2008.
37. Li J, Hart RP, Mallimo EM, Swerdel MR, Kusnecov AW, Herrup K. EZH2-mediated H3K27 trimethylation mediates neurodegeneration in ataxia-telangiectasia. Nat Neurosci 2013; 16: 1745–1753.
38. Marin-Bejar O, Marchese FP, Athie A, Sanchez Y, Gonzalez J, Segura V et al. Pint lincRNA connects the p53 pathway with epigenetic silencing by the Polycomb repressive complex 2. Genome Biol 2013; 14: R104.
39. Luckey CJ, Bhattacharya D, Goldrath AW, Weissman IL, Benoist C, Mathis D. Memory T and memory B cells share a transcriptional program of self-renewal with long-term hematopoietic stem cells. Proc Natl Acad Sci USA 2006; 103: 3304–3309.