Genome-wide signatures of differential DNA methylation in pediatric acute lymphoblastic leukemia

Genome Biology

Volumn 14, Issue 9, 2013, Pages

  Nordlund, Jessica ^a   Bäcklin, Christofer L ^a   Wahlberg, Per ^a   Busche, Stephan ^b   Berglund, Eva C ^a   Eloranta, Maija Leena ^a   Flaegstad, Trond ^c   Forestier, Erik ^d   Frost, Britt Marie ^a   Harila Saari, Arja ^e,f   Heyman, Mats ^f   Jónsson, Ólafur G ^g   Larsson, Rolf ^a   Palle, Josefine ^a   Rönnblom, Lars ^a   Schmiegelow, Kjeld ^h   Sinnett, Daniel ⁱ   Söderhäll, Stefan ^a   Pastinen, Tomi ^b   Gustafsson, Mats G ^a   Lönnerholm, Gudmar ^a   Syvänen, Ann Christine ^a   more..

^a UPPSALA UNIVERSITY   (Sweden)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF TROMSØ   (Norway)

^d UMEÅ UNIVERSITY   (Sweden)

^e OULU UNIVERSITY HOSPITAL   (Finland)

^f KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^g LANDSPITALI UNIVERSITY HOSPITAL   (Iceland)

^h UNIVERSITY OF COPENHAGEN   (Denmark)

ⁱ UNIVERSITY OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; ZINC FINGER PROTEIN; ANTINEOPLASTIC AGENT; CHROMATIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; CD3+ T LYMPHOCYTE; CD34 SELECTION; CHILD; CHILDHOOD LEUKEMIA; CHROMATIN; CONTROLLED STUDY; CPG ISLAND; CYTOGENETICS; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; INTRON; LEUKEMIA RELAPSE; MAJOR CLINICAL STUDY; MALE; PRESCHOOL CHILD; PROMOTER REGION; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; RISK FACTOR; ADOLESCENT; CHEMISTRY; CHROMOSOME ABERRATION; DISEASE FREE SURVIVAL; ENHANCER REGION; GENE EXPRESSION PROFILING; GENETICS; HUMAN GENOME; METABOLISM; MORTALITY; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROGNOSIS; RECURRENT DISEASE; RISK;

ADOLESCENT; ANTINEOPLASTIC AGENTS; CHILD; CHILD, PRESCHOOL; CHROMATIN; CHROMOSOME ABERRATIONS; CPG ISLANDS; DISEASE-FREE SURVIVAL; DNA METHYLATION; ENHANCER ELEMENTS, GENETIC; FEMALE; GENE EXPRESSION PROFILING; GENOME, HUMAN; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROGNOSIS; PROMOTER REGIONS, GENETIC; RECURRENCE; RISK;

EID: 84884898098     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2013-14-9-r105     Document Type: Article

References (55)

1. Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev 2011, 25:1010-1022.
2. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012, 13:484-492.
3. Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol 2010, 28:1057-1068.
4. You JS, Jones PA. Cancer genetics and epigenetics: two sides of the same coin?. Cancer Cell 2012, 22:9-20.
5. Schmiegelow K, Forestier E, Hellebostad M, Heyman M, Kristinsson J, Soderhall S, Taskinen M. Long-term results of NOPHO ALL-92 and ALL-2000 studies of childhood acute lymphoblastic leukemia. Leukemia 2010, 24:345-354.
6. Pui CH, Carroll WL, Meshinchi S, Arceci RJ. Biology, risk stratification, and therapy of pediatric acute leukemias: an update. J Clin Oncol 2011, 29:551-565.
7. Nordlund J, Milani L, Lundmark A, Lonnerholm G, Syvanen AC. DNA methylation analysis of bone marrow cells at diagnosis of acute lymphoblastic leukemia and at remission. PLoS One 2012, 7:e34513.
8. Wong NC, Ashley D, Chatterton Z, Parkinson-Bates M, Ng HK, Halemba MS, Kowalczyk A, Bedo J, Wang Q, Bell K, Algar E, Craig JM, Saffery R. A distinct DNA methylation signature defines pediatric pre-B cell acute lymphoblastic leukemia. Epigenetics 2012, 7:535-541.
9. Geng H, Brennan S, Milne TA, Chen WY, Li Y, Hurtz C, Kweon SM, Zickl L, Shojaee S, Neuberg D, Huang C, Biswas D, Xin Y, Racevskis J, Ketterling RP, Luger SM, Lazarus H, Tallman MS, Rowe JM, Litzow MR, Guzman ML, Allis CD, Roeder RG, Müschen M, Paietta E, Elemento O, Melnick AM. Integrative epigenomic analysis identifies biomarkers and therapeutic targets in adult B-acute lymphoblastic leukemia. Cancer Discov 2012, 2:1004-1023.
10. Milani L, Lundmark A, Kiialainen A, Nordlund J, Flaegstad T, Forestier E, Heyman M, Jonmundsson G, Kanerva J, Schmiegelow K, Söderhäll S, Gustafsson MG, Lönnerholm G, Syvänen AC. DNA methylation for subtype classification and prediction of treatment outcome in patients with childhood acute lymphoblastic leukemia. Blood 2010, 115:1214-1225.
11. Davidsson J, Lilljebjorn H, Andersson A, Veerla S, Heldrup J, Behrendtz M, Fioretos T, Johansson B. The DNA methylome of pediatric acute lymphoblastic leukemia. Hum Mol Genet 2009, 18:4054-4065.
12. Busche S, Ge B, Vidal R, Spinella J-F, Saillour V, Richer C, Healy J, Chen S-H, Droit A, Sinnett D, Pastinen T. Integration of high-resolution methylome and transcriptome analyses to dissect epigenomic changes in childhood acute lymphoblastic leukemia. Cancer Res 2013, 73:4323-4336.
13. Hogan LE, Meyer JA, Yang J, Wang J, Wong N, Yang W, Condos G, Hunger SP, Raetz E, Saffery R, Relling MV, Bhojwani D, Morrison DJ, Carroll WL. Integrated genomic analysis of relapsed childhood acute lymphoblastic leukemia reveals therapeutic strategies. Blood 2011, 118:5218-5226.
14. Bhatla T, Wang J, Morrison DJ, Raetz EA, Burke MJ, Brown P, Carroll WL. Epigenetic reprogramming reverses the relapse-specific gene expression signature and restores chemosensitivity in childhood B-lymphoblastic leukemia. Blood 2012, 119:5201-5210.
15. Pui CH, Mullighan CG, Evans WE, Relling MV. Pediatric acute lymphoblastic leukemia: where are we going and how do we get there?. Blood 2012, 120:1165-1174.
16. Figueroa ME, Chen S-C, Andersson AK, Phillips LA, Li Y, Sotzen J, Kundu M, Downing JR, Melnick A, Mullighan CG. Integrated genetic and epigenetic analysis of childhood acute lymphoblastic leukemia. J Clin Invest 2013, 123:3099-3111.
17. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, Kellis M, Marra MA, Beaudet AL, Ecker JR, Farnham PJ, Hirst M, Lander ES, Mikkelsen TS, Thomson JA. The NIH roadmap epigenomics mapping consortium. Nat Biotechnol 2010, 28:1045-1048.
18. ENCODE Project Consortium A user's guide to the encyclopedia of DNA elements (ENCODE). Plos Biol 2011, 9:e1001046. ENCODE Project Consortium.
19. Nordlund J, Kiialainen A, Karlberg O, Berglund EC, Göransson-Kultima H, Sønderkær M, Nielsen KL, Gustafsson MG, Behrendtz M, Forestier E, Perkkiö M, Söderhäll S, Lönnerholm G, Syvänen AC. Digital gene expression profiling of primary acute lymphoblastic leukemia cells. Leukemia 2012, 26:1218-1227.
20. Bostick M, Kim JK, Esteve PO, Clark A, Pradhan S, Jacobsen SE. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 2007, 317:1760-1764.
21. Watson PJ, Fairall L, Schwabe JWR. Nuclear hormone receptor co-repressors: structure and function. Mol Cell Endocrinol 2012, 348:440-449.
22. Ross ME, Zhou X, Song G, Shurtleff SA, Girtman K, Williams WK, Liu HC, Mahfouz R, Raimondi SC, Lenny N, Patel A, Downing J. Classification of pediatric acute lymphoblastic leukemia by gene expression profiling. Blood 2003, 102:2951-2959.
23. Tibshirani R, Hastie T, Narasimhan B, Chu G. Class prediction by nearest shrunken centroids, with applications to DNA microarrays. Stat Sci 2003, 18:104-117.
24. Patzke S, Lindeskog M, Munthe E, Aasheim HC. Characterization of a novel human endogenous retrovirus, HERV-H/F, expressed in human leukemia cell lines. Virology 2002, 303:164-173.
25. Holmfeldt L, Wei L, Diaz-Flores E, Walsh M, Zhang J, Ding L, Payne-Turner D, Churchman M, Andersson A, Chen SC, McCastlain K, Becksfort J, Ma J, Wu G, Patel SN, Heatley SL, Phillips LA, Song G, Easton J, Parker M, Chen X, Rusch M, Boggs K, Vadodaria B, Hedlund E, Drenberg C, Baker S, Pei D, Cheng C, Huether R, et al. The genomic landscape of hypodiploid acute lymphoblastic leukemia. Nat Genet 2013, 45:242-252.
26. Staffas A, Kanduri M, Hovland R, Rosenquist R, Ommen HB, Abrahamsson J, Forestier E, Jahnukainen K, Jónsson T, Zeller B, Palle J, Lönnerholm G, Hasle H, Palmqvist L, Ehrencrona H, Nordic Society of Pediatric Hematology and Oncology (NOPHO) Presence of FLT3-ITD and high BAALC expression are independent prognostic markers in childhood acute myeloid leukemia. Blood 2011, 118:5905-5913. Nordic Society of Pediatric Hematology and Oncology (NOPHO).
27. Lin PC, Giannopoulou EG, Park K, Mosquera JM, Sboner A, Tewari AK, Garraway LA, Beltran H, Rubin MA, Elemento O. Epigenomic alterations in localized and advanced prostate cancer. Neoplasia 2013, 15:373-383.
28. Milani L, Lundmark A, Nordlund J, Kiialainen A, Flaegstad T, Jonmundsson G, Kanerva J, Schmiegelow K, Gunderson KL, Lonnerholm G, Syvanen AC. Allele-specific gene expression patterns in primary leukemic cells reveal regulation of gene expression by CpG site methylation. Genome Res 2009, 19:1-11.
29. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, Mohammad HP, Chen W, Daniel VC, Yu W, Berman DM, Jenuwein T, Pruitt K, Sharkis SJ, Watkins DN, Herman JG, Baylin SB. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 2007, 39:237-242.
30. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, Ku M, Durham T, Kellis M, Bernstein BE. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 2011, 473:43-49.
31. Easwaran H, Johnstone SE, Van Neste L, Ohm J, Mosbruger T, Wang Q, Aryee MJ, Joyce P, Ahuja N, Weisenberger D, Collisson E, Zhu J, Yegnasubramanian S, Matsui W, Baylin SB. A DNA hypermethylation module for the stem/progenitor cell signature of cancer. Genome Res 2012, 22:837-849.
32. Ammerpohl O, Haake A, Pellissery S, Giefing M, Richter J, Balint B, Kulis M, Le J, Bibikova M, Drexler HG, Seifert M, Shaknovic R, Korn B, Küppers R, Martín-Subero JI, Siebert R. Array-based DNA methylation analysis in classical Hodgkin lymphoma reveals new insights into the mechanisms underlying silencing of B cell-specific genes. Leukemia 2012, 26:185-188.
33. Deneberg S, Guardiola P, Lennartsson A, Qu Y, Gaidzik V, Blanchet O, Karimi M, Bengtzén S, Nahi H, Uggla B, Tidefelt U, Höglund M, Paul C, Ekwall K, Döhner K, Lehmann S. Prognostic DNA methylation patterns in cytogenetically normal acute myeloid leukemia are predefined by stem cell chromatin marks. Blood 2011, 118:5573-5582.
34. Gal-Yam EN, Egger G, Iniguez L, Holster H, Einarsson S, Zhang X, Lin JC, Liang G, Jones PA, Tanay A. Frequent switching of Polycomb repressive marks and DNA hypermethylation in the PC3 prostate cancer cell line. Proc Natl Acad Sci USA 2008, 105:12979-12984.
35. Stumpel DJ, Schneider P, van Roon EH, Boer JM, de Lorenzo P, Valsecchi MG, de Menezes RX, Pieters R, Stam RW. Specific promoter methylation identifies different subgroups of MLL-rearranged infant acute lymphoblastic leukemia, influences clinical outcome, and provides therapeutic options. Blood 2009, 114:5490-5498.
36. Schafer E, Irizarry R, Negi S, McIntyre E, Small D, Figueroa ME, Melnick A, Brown P. Promoter hypermethylation in MLL-r infant acute lymphoblastic leukemia: biology and therapeutic targeting. Blood 2010, 115:4798-4809.
37. Jelinek J, Gharibyan V, Estecio MR, Kondo K, He R, Chung W, Lu Y, Zhang N, Liang S, Kantarjian HM, Cortes JE, Issa JP. Aberrant DNA methylation is associated with disease progression, resistance to imatinib and shortened survival in chronic myelogenous leukemia. PLoS One 2011, 6:e22110.
38. De Carvalho DD, Sharma S, You JS, Su SF, Taberlay PC, Kelly TK, Yang X, Liang G, Jones PA. DNA methylation screening identifies driver epigenetic events of cancer cell survival. Cancer Cell 2012, 21:655-667.
39. Shen H, Laird PW. In epigenetic therapy, less is more. Cell Stem Cell 2012, 10:353-354.
40. Kulis M, Heath S, Bibikova M, Queirós AC, Navarro A, Clot G, Martínez-Trillos A, Castellano G, Brun-Heath I, Pinyol M, Barberán-Soler S, Papasaikas P, Jares P, Beà S, Rico D, Ecker S, Rubio M, Royo R, Ho V, Klotzle B, Hernández L, Conde L, López-Guerra M, Colomer D, Villamor N, Aymerich M, Rozman M, Bayes M, Gut M, Gelpí JL, et al. Epigenomic analysis detects widespread gene-body DNA hypomethylation in chronic lymphocytic leukemia. Nat Genet 2012, 44:1236-1242.
41. Schmidl C, Klug M, Boeld TJ, Andreesen R, Hoffmann P, Edinger M, Rehli M. Lineage-specific DNA methylation in T cells correlates with histone methylation and enhancer activity. Genome Res 2009, 19:1165-1174.
42. Aran D, Sabato S, Hellman A. DNA methylation of distal regulatory sites characterizes dysregulation of cancer genes. Genome Biol 2013, 14:R21.
43. Esteller M. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents (vol 343, pg 1350, 2000). New Engl J Med 2000, 343:1740-1740.
44. Tan AC, Jimeno A, Lin SH, Wheelhouse J, Chan F, Solomon A, Rajeshkumar NV, Rubio-Viqueira B, Hidalgo M. Characterizing DNA methylation patterns in pancreatic cancer genome. Mol Oncol 2009, 3:425-438.
45. Toft N, Birgens H, Abrahamsson J, Bernell P, Griškevičius L, Hallböök H, Heyman M, Holm MS, Hulegårdh E, Klausen TW, Marquart HV, Jónsson OG, Nielsen OJ, Quist-Paulsen P, Taskinen M, Vaitkeviciene G, Vettenranta K, Åsberg A, Schmiegelow K. Risk group assignment differs for children and adults 1-45 yr with acute lymphoblastic leukemia treated by the NOPHO ALL-2008 protocol. Euro J Haematol 2013, 90:404-412.
46. Romanish MT, Cohen CJ, Mager DL. Potential mechanisms of endogenous retroviral-mediated genomic instability in human cancer. Semin Cancer Biol 2010, 20:246-253.
47. Klco JM, Spencer DH, Lamprecht TL, Sarkaria SM, Wylie T, Magrini V, Hundal J, Walker J, Varghese N, Erdmann-Gilmore P, Lichti CF, Meyer MR, Townsend RR, Wilson RK, Mardis ER, Ley TJ. Genomic impact of transient low-dose decitabine treatment on primary AML cells. Blood 2013, 121:1633-1643.
48. 3H Biomedical [http://www.3hbiomedical.com/].
49. Dedeurwaerder S, Defrance M, Calonne E, Denis H, Sotiriou C, Fuks F. Evaluation of the Infinium Methylation 450K technology. Epigenomics 2011, 3:771-784.
50. Feng J, Liu T, Zhang Y. Using MACS to identify peaks from ChIP-Seq data. Curr Protoc Bioinformatics 2011, 34:2.14.1-2.14.14.
51. UCSC Genome Browser [http://genome.ucsc.edu].
52. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
53. Benjamini Y, Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 1995, 57:289-300.
54. R Core Development Team R: A Language and Environment for Statistical Computing 2011, Vienna, Austria: R Foundation for Statistical Computing, R Core Development Team.
55. GitHub [https://github.com/Molmed/Nordlund-Backlin-2013].