DNA methylation dynamics during B cell maturation underlie a continuum of disease phenotypes in chronic lymphocytic leukemia

Christoph Plass, Christopher Oakes and colleagues study genome-wide DNA methylation dynamics during B cell maturation and the pathogenic role of transcription factor dysregulation in chronic lymphocytic leukemia (CLL). By comparing normal and malignant B cells, they find that tumors derive from a co...

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Published inNature genetics Vol. 48; no. 3; pp. 253 - 264
Main Authors Oakes, Christopher C, Seifert, Marc, Assenov, Yassen, Gu, Lei, Przekopowitz, Martina, Ruppert, Amy S, Wang, Qi, Imbusch, Charles D, Serva, Andrius, Koser, Sandra D, Brocks, David, Lipka, Daniel B, Bogatyrova, Olga, Weichenhan, Dieter, Brors, Benedikt, Rassenti, Laura, Kipps, Thomas J, Mertens, Daniel, Zapatka, Marc, Lichter, Peter, Döhner, Hartmut, Küppers, Ralf, Zenz, Thorsten, Stilgenbauer, Stephan, Byrd, John C, Plass, Christoph
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.03.2016
Nature Publishing Group
Subjects
13/1
13/106
38/91
45/22
45/23
45/90
631/208/177
692/699/67/1990/283/1895
Adult
Aged
Aged, 80 and over
Agriculture
Animal Genetics and Genomics
B cells
B-Lymphocytes - immunology
B-Lymphocytes - metabolism
Binding Sites
Biomedicine
Cancer
Cancer Research
Chronic lymphocytic leukemia
Consortia
CpG Islands - genetics
Deoxyribonucleic acid
Development and progression
Developmental stages
DNA
DNA methylation
DNA Methylation - genetics
Epigenesis, Genetic
Epigenetic inheritance
Epigenetics
Female
Gene expression
Gene Expression Regulation, Leukemic
Gene Expression Regulation, Neoplastic
Gene Function
Genetic aspects
Genomes
Growth
Health aspects
Human Genetics
Humans
Leukemia
Leukemia, Lymphocytic, Chronic, B-Cell - genetics
Leukemia, Lymphocytic, Chronic, B-Cell - immunology
Leukemia, Lymphocytic, Chronic, B-Cell - pathology
Male
Medical research
Middle Aged
Neoplasm Proteins - biosynthesis
Neoplasm Proteins - genetics
Phenotype
Promoter Regions, Genetic
Software
Transcription factors
Tumors
Online AccessGet full text

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Abstract Christoph Plass, Christopher Oakes and colleagues study genome-wide DNA methylation dynamics during B cell maturation and the pathogenic role of transcription factor dysregulation in chronic lymphocytic leukemia (CLL). By comparing normal and malignant B cells, they find that tumors derive from a continuum of maturation states, which correlate with different clinical outcomes. Charting differences between tumors and normal tissue is a mainstay of cancer research. However, clonal tumor expansion from complex normal tissue architectures potentially obscures cancer-specific events, including divergent epigenetic patterns. Using whole-genome bisulfite sequencing of normal B cell subsets, we observed broad epigenetic programming of selective transcription factor binding sites coincident with the degree of B cell maturation. By comparing normal B cells to malignant B cells from 268 patients with chronic lymphocytic leukemia (CLL), we showed that tumors derive largely from a continuum of maturation states reflected in normal developmental stages. Epigenetic maturation in CLL was associated with an indolent gene expression pattern and increasingly favorable clinical outcomes. We further uncovered that most previously reported tumor-specific methylation events are normally present in non-malignant B cells. Instead, we identified a potential pathogenic role for transcription factor dysregulation in CLL, where excess programming by EGR and NFAT with reduced EBF and AP-1 programming imbalances the normal B cell epigenetic program.
AbstractList Charting differences between tumors and normal tissue is a mainstay of cancer research. However, clonal tumor expansion from complex normal tissue architectures potentially obscures cancer-specific events, including divergent epigenetic patterns. Using whole-genome bisulfite sequencing of normal B cell subsets, we observed broad epigenetic programming of selective transcription factor binding sites coincident with the degree of B cell maturation. By comparing normal B cells to malignant B cells from 268 patients with chronic lymphocytic leukemia (CLL), we showed that tumors derive largely from a continuum of maturation states reflected in normal developmental stages. Epigenetic maturation in CLL was associated with an indolent gene expression pattern and increasingly favorable clinical outcomes. We further uncovered that most previously reported tumor-specific methylation events are normally present in non-malignant B cells. Instead, we identified a potential pathogenic role for transcription factor dysregulation in CLL, where excess programming by EGR and NFAT with reduced EBF and AP-1 programming imbalances the normal B cell epigenetic program.
Charting differences between tumors and normal tissue is a mainstay of cancer research. However, clonal tumor expansion from complex normal tissue architectures potentially obscures cancer-specific events, including divergent epigenetic patterns. Using whole-genome bisulfite sequencing of normal B cell subsets, we observed broad epigenetic programming of selective transcription factor binding sites coincident with the degree of B cell maturation. By comparing normal B cells to malignant B cells from 268 patients with chronic lymphocytic leukemia (CLL), we showed that tumors derive largely from a continuum of maturation states reflected in normal developmental stages. Epigenetic maturation in CLL was associated with an indolent gene expression pattern and increasingly favorable clinical outcomes. We further uncovered that most previously reported tumor-specific methylation events are normally present in non-malignant B cells. Instead, we identified a potential pathogenic role for transcription factor dysregulation in CLL, where excess programming by EGR and NFAT with reduced EBF and AP-1 programming imbalances the normal B cell epigenetic program.Charting differences between tumors and normal tissue is a mainstay of cancer research. However, clonal tumor expansion from complex normal tissue architectures potentially obscures cancer-specific events, including divergent epigenetic patterns. Using whole-genome bisulfite sequencing of normal B cell subsets, we observed broad epigenetic programming of selective transcription factor binding sites coincident with the degree of B cell maturation. By comparing normal B cells to malignant B cells from 268 patients with chronic lymphocytic leukemia (CLL), we showed that tumors derive largely from a continuum of maturation states reflected in normal developmental stages. Epigenetic maturation in CLL was associated with an indolent gene expression pattern and increasingly favorable clinical outcomes. We further uncovered that most previously reported tumor-specific methylation events are normally present in non-malignant B cells. Instead, we identified a potential pathogenic role for transcription factor dysregulation in CLL, where excess programming by EGR and NFAT with reduced EBF and AP-1 programming imbalances the normal B cell epigenetic program.
Christoph Plass, Christopher Oakes and colleagues study genome-wide DNA methylation dynamics during B cell maturation and the pathogenic role of transcription factor dysregulation in chronic lymphocytic leukemia (CLL). By comparing normal and malignant B cells, they find that tumors derive from a continuum of maturation states, which correlate with different clinical outcomes. Charting differences between tumors and normal tissue is a mainstay of cancer research. However, clonal tumor expansion from complex normal tissue architectures potentially obscures cancer-specific events, including divergent epigenetic patterns. Using whole-genome bisulfite sequencing of normal B cell subsets, we observed broad epigenetic programming of selective transcription factor binding sites coincident with the degree of B cell maturation. By comparing normal B cells to malignant B cells from 268 patients with chronic lymphocytic leukemia (CLL), we showed that tumors derive largely from a continuum of maturation states reflected in normal developmental stages. Epigenetic maturation in CLL was associated with an indolent gene expression pattern and increasingly favorable clinical outcomes. We further uncovered that most previously reported tumor-specific methylation events are normally present in non-malignant B cells. Instead, we identified a potential pathogenic role for transcription factor dysregulation in CLL, where excess programming by EGR and NFAT with reduced EBF and AP-1 programming imbalances the normal B cell epigenetic program.
Audience Academic
Author Kipps, Thomas J
Plass, Christoph
Stilgenbauer, Stephan
Byrd, John C
Döhner, Hartmut
Mertens, Daniel
Assenov, Yassen
Küppers, Ralf
Gu, Lei
Koser, Sandra D
Imbusch, Charles D
Bogatyrova, Olga
Lipka, Daniel B
Rassenti, Laura
Seifert, Marc
Weichenhan, Dieter
Ruppert, Amy S
Serva, Andrius
Zapatka, Marc
Przekopowitz, Martina
Zenz, Thorsten
Wang, Qi
Brocks, David
Lichter, Peter
Oakes, Christopher C
Brors, Benedikt
AuthorAffiliation 2 Institute of Cell Biology (Cancer Research), University of Duisburg-Essen, Essen, Germany
7 Division of Applied Bioinformatics, German Cancer Research Center (DKFZ), Heidelberg, Germany
5 Division of Hematology, Department of Internal Medicine, The Ohio State University, Columbus, Ohio, USA
10 Cooperation Unit Mechanisms of Leukemogenesis, German Cancer Research Center (DKFZ), Heidelberg, Germany
8 Division of Molecular Genetics, German Cancer Research Center (DKFZ), Heidelberg, Germany
1 Division of Epigenomics and Cancer Risk Factors, German Cancer Research Center (DKFZ), Heidelberg, Germany
4 Division of Newborn Medicine, Boston Children’s Hospital, Boston, Massachusetts, USA
6 Division of Theoretical Bioinformatics, German Cancer Research Center (DKFZ), Heidelberg, Germany
11 Department of Internal Medicine III, University of Ulm, Ulm, Germany
3 Department of Cell Biology, Harvard Medical School, Boston, Massachusetts, USA
9 Department of Medicine, University of California at San Diego Moo
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/26780610$$D View this record in MEDLINE/PubMed
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Cites_doi 10.1084/jem.194.11.1625
10.1182/blood-2012-01-402453
10.1182/blood-2010-05-284984
10.1038/nprot.2013.118
10.1038/ng.3413
10.1089/106652702761034136
10.1182/blood.V100.4.1410.h81602001410_1410_1416
10.1038/leu.2012.280
10.1111/j.1365-2141.2010.08299.x
10.1038/nature09906
10.1158/2159-8290.CD-13-0349
10.1182/blood-2014-02-555722
10.2217/epi.11.73
10.1038/nrc3486
10.1016/j.semcancer.2010.09.004
10.1016/j.ccell.2014.10.012
10.1182/blood-2011-06-357996
10.1038/nmeth.3115
10.1016/j.celrep.2014.06.053
10.1126/science.1242510
10.1038/ng.2443
10.1073/pnas.0810965105
10.1038/nature10113
10.1038/nature14192
10.1101/gr.103606.109
10.4049/jimmunol.181.5.3364
10.1038/bcj.2015.14
10.1016/0092-8674(94)90076-0
10.1016/j.stem.2014.07.005
10.1084/jem.188.9.1679
10.1182/blood-2006-11-056648
10.1093/bioinformatics/btp698
10.1084/jem.20101947
10.1038/nbt.1630
10.1038/nature12433
10.1016/S1074-7613(01)00085-1
10.1084/jem.20120833
10.1093/nar/gkt1323
10.1182/blood-2012-04-423517
10.1158/2159-8290.CD-14-0104
10.1182/blood-2006-12-062265
10.1016/S1074-7613(00)80040-0
10.1084/jem.185.3.563
10.1016/j.ccr.2012.08.024
10.1101/gr.155473.113
10.1038/leu.2014.252
10.4049/jimmunol.181.7.4590
10.1038/nature12787
10.1126/science.1256271
10.1016/j.exphem.2014.04.012
10.1016/j.cell.2013.01.019
10.1101/gr.152132.112
10.2217/epi.09.14
10.1073/pnas.1413374111
10.1038/leu.2012.245
10.1038/ng.3291
10.1093/bioinformatics/bts680
10.1073/pnas.0506580102
10.1126/science.1105136
10.1038/nrg3354
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References Ernst (CR20) 2011; 473
Ferreira (CR29) 2014; 24
Kröber (CR51) 2002; 100
Kasowski (CR5) 2013; 342
Wang (CR17) 2013; 8
Klein (CR39) 2001; 194
Ziller (CR3) 2013; 500
Cabezas-Wallscheid (CR7) 2014; 15
Sturm (CR36) 2012; 22
Bibikova (CR53) 2009; 1
Bohle, Döring, Hansmann, Küppers (CR60) 2013; 27
Kretzmer (CR43) 2015; 47
Li, Durbin (CR52) 2010; 26
Florean, Schnekenburger, Grandjenette, Dicato, Diederich (CR22) 2011; 3
Rosén, Murray, Evaldsson, Rosenquist (CR49) 2010; 20
Pekarsky (CR50) 2008; 105
Teschendorff (CR55) 2013; 29
Andersson (CR1) 2014; 507
Lara-Astiaso (CR6) 2014; 345
Peng, Gerth, Ranger, Glimcher (CR46) 2001; 14
Kulis (CR15) 2015; 47
CR2
Shaknovich (CR18) 2011; 118
Cahill (CR12) 2013; 27
Queiros (CR11) 2015; 29
Puente (CR30) 2011; 475
Timp, Feinberg (CR9) 2013; 13
Landau (CR14) 2014; 26
Lai (CR19) 2013; 23
Schübeler (CR8) 2015; 517
Desper, Gascuel (CR58) 2002; 9
Oakes (CR13) 2014; 4
Pham (CR37) 2012; 119
Seifert (CR28) 2012; 209
Assenov (CR56) 2014; 11
Gustems (CR48) 2014; 42
Zhuang, Soriano, Weintraub (CR44) 1994; 79
Chen (CR41) 2008; 111
Kulis (CR10) 2012; 44
Reindl (CR34) 2010; 151
Zandi (CR26) 2008; 181
Klein, Rajewsky, Küppers (CR40) 1998; 188
Herishanu (CR32) 2011; 117
Landau (CR31) 2013; 152
Brocks (CR57) 2014; 8
Edelmann (CR35) 2012; 120
Heltemes-Harris (CR27) 2011; 208
Gururajan (CR45) 2008; 181
CR54
Smith, Meissner (CR4) 2013; 14
Mockridge (CR33) 2007; 109
Claus (CR25) 2014; 124
Dvinge (CR21) 2014; 111
Prange, Singh, Martens (CR42) 2014; 42
Teschendorff (CR23) 2010; 20
Smith (CR24) 2015; 5
McLean (CR61) 2010; 28
Subramanian (CR59) 2005; 102
Garrett-Sinha (CR47) 1999; 10
Damm (CR38) 2014; 4
Lebecque, de Bouteiller, Arpin, Banchereau, Liu (CR16) 1997; 185
AY Lai (BFng3488_CR19) 2013; 23
M Bibikova (BFng3488_CR53) 2009; 1
AE Teschendorff (BFng3488_CR23) 2010; 20
D Lara-Astiaso (BFng3488_CR6) 2014; 345
R Andersson (BFng3488_CR1) 2014; 507
D Sturm (BFng3488_CR36) 2012; 22
Q Wang (BFng3488_CR17) 2013; 8
XS Puente (BFng3488_CR30) 2011; 475
R Desper (BFng3488_CR58) 2002; 9
EN Smith (BFng3488_CR24) 2015; 5
Y Herishanu (BFng3488_CR32) 2011; 117
M Gururajan (BFng3488_CR45) 2008; 181
BFng3488_CR54
LA Garrett-Sinha (BFng3488_CR47) 1999; 10
D Brocks (BFng3488_CR57) 2014; 8
M Seifert (BFng3488_CR28) 2012; 209
A Rosén (BFng3488_CR49) 2010; 20
DA Landau (BFng3488_CR31) 2013; 152
AE Teschendorff (BFng3488_CR55) 2013; 29
A Subramanian (BFng3488_CR59) 2005; 102
CC Oakes (BFng3488_CR13) 2014; 4
AC Queiros (BFng3488_CR11) 2015; 29
U Klein (BFng3488_CR39) 2001; 194
PG Ferreira (BFng3488_CR29) 2014; 24
TH Pham (BFng3488_CR37) 2012; 119
SL Peng (BFng3488_CR46) 2001; 14
J Ernst (BFng3488_CR20) 2011; 473
M Kulis (BFng3488_CR10) 2012; 44
H Li (BFng3488_CR52) 2010; 26
S Lebecque (BFng3488_CR16) 1997; 185
Y Assenov (BFng3488_CR56) 2014; 11
DA Landau (BFng3488_CR14) 2014; 26
J Edelmann (BFng3488_CR35) 2012; 120
CI Mockridge (BFng3488_CR33) 2007; 109
A Kröber (BFng3488_CR51) 2002; 100
L Reindl (BFng3488_CR34) 2010; 151
BFng3488_CR2
LM Heltemes-Harris (BFng3488_CR27) 2011; 208
V Bohle (BFng3488_CR60) 2013; 27
R Claus (BFng3488_CR25) 2014; 124
KH Prange (BFng3488_CR42) 2014; 42
Y Zhuang (BFng3488_CR44) 1994; 79
H Kretzmer (BFng3488_CR43) 2015; 47
M Kasowski (BFng3488_CR5) 2013; 342
MJ Ziller (BFng3488_CR3) 2013; 500
Y Pekarsky (BFng3488_CR50) 2008; 105
H Dvinge (BFng3488_CR21) 2014; 111
L Chen (BFng3488_CR41) 2008; 111
CY McLean (BFng3488_CR61) 2010; 28
N Cabezas-Wallscheid (BFng3488_CR7) 2014; 15
M Kulis (BFng3488_CR15) 2015; 47
S Zandi (BFng3488_CR26) 2008; 181
W Timp (BFng3488_CR9) 2013; 13
R Shaknovich (BFng3488_CR18) 2011; 118
ZD Smith (BFng3488_CR4) 2013; 14
D Schübeler (BFng3488_CR8) 2015; 517
M Gustems (BFng3488_CR48) 2014; 42
U Klein (BFng3488_CR40) 1998; 188
N Cahill (BFng3488_CR12) 2013; 27
C Florean (BFng3488_CR22) 2011; 3
F Damm (BFng3488_CR38) 2014; 4
24071908 - Nat Protoc. 2013 Oct;8(10):2022-32
25103404 - Science. 2014 Aug 22;345(6199):943-9
18048647 - Blood. 2008 Mar 1;111(5):2685-92
20863893 - Semin Cancer Biol. 2010 Dec;20(6):400-9
25158935 - Cell Stem Cell. 2014 Oct 2;15(4):507-22
26437030 - Nat Genet. 2015 Nov;47(11):1316-25
17255355 - Blood. 2007 May 15;109(10):4424-31
24868078 - Blood. 2014 Jul 3;124(1):42-8
12149225 - Blood. 2002 Aug 15;100(4):1410-6
11163226 - Immunity. 2001 Jan;14(1):13-20
25151957 - Leukemia. 2015 Mar;29(3):598-605
9802980 - J Exp Med. 1998 Nov 2;188(9):1679-89
25385641 - Proc Natl Acad Sci U S A. 2014 Nov 25;111(47):16802-7
25262207 - Nat Methods. 2014 Nov;11(11):1138-40
23064414 - Nat Genet. 2012 Nov;44(11):1236-42
22922567 - Leukemia. 2013 Jan;27(1):150-8
20649559 - Br J Haematol. 2010 Oct;151(1):25-36
25860294 - Blood Cancer J. 2015 Apr 10;5:e303
24136358 - Science. 2013 Nov 8;342(6159):750-2
21642962 - Nature. 2011 Jun 05;475(7354):101-5
23175756 - Bioinformatics. 2013 Jan 15;29(2):189-96
23174882 - Leukemia. 2013 Mar;27(3):671-9
23925113 - Nature. 2013 Aug 22;500(7463):477-81
23400093 - Nat Rev Genet. 2013 Mar;14(3):204-20
24920063 - Cancer Discov. 2014 Sep;4(9):1088-101
20219944 - Genome Res. 2010 Apr;20(4):440-6
9053456 - J Exp Med. 1997 Feb 3;185(3):563-71
23760024 - Nat Rev Cancer. 2013 Jul;13(7):497-510
20940416 - Blood. 2011 Jan 13;117(2):563-74
26053498 - Nat Genet. 2015 Jul;47(7):746-56
19064921 - Proc Natl Acad Sci U S A. 2008 Dec 16;105(50):19643-8
16199517 - Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50
21441907 - Nature. 2011 May 5;473(7345):43-9
23047824 - Blood. 2012 Dec 6;120(24):4783-94
18802061 - J Immunol. 2008 Oct 1;181(7):4590-602
21606506 - J Exp Med. 2011 Jun 6;208(6):1135-49
22550342 - Blood. 2012 Jun 14;119(24):e161-71
22122642 - Epigenomics. 2009 Oct;1(1):177-200
10229183 - Immunity. 1999 Apr;10(4):399-408
21828137 - Blood. 2011 Sep 29;118(13):3559-69
23079654 - Cancer Cell. 2012 Oct 16;22(4):425-37
24371273 - Nucleic Acids Res. 2014 Mar;42(5):3059-72
24356097 - Cancer Discov. 2014 Mar;4(3):348-61
25693563 - Nature. 2015 Feb 19;518(7539):317-30
23415222 - Cell. 2013 Feb 14;152(4):714-26
25066126 - Cell Rep. 2014 Aug 7;8(3):798-806
23091163 - J Exp Med. 2012 Nov 19;209(12):2183-98
24814246 - Exp Hematol. 2014 Aug;42(8):637-50
12487758 - J Comput Biol. 2002;9(5):687-705
24013550 - Genome Res. 2013 Dec;23(12):2030-41
25490447 - Cancer Cell. 2014 Dec 8;26(6):813-25
15499007 - Science. 2004 Oct 22;306(5696):636-40
20436461 - Nat Biotechnol. 2010 May;28(5):495-501
11733577 - J Exp Med. 2001 Dec 3;194(11):1625-38
22126248 - Epigenomics. 2011 Oct;3(5):581-609
25592537 - Nature. 2015 Jan 15;517(7534):321-6
24265505 - Genome Res. 2014 Feb;24(2):212-26
24670763 - Nature. 2014 Mar 27;507(7493):455-61
20080505 - Bioinformatics. 2010 Mar 1;26(5):589-95
18714008 - J Immunol. 2008 Sep 1;181(5):3364-72
8001124 - Cell. 1994 Dec 2;79(5):875-84
References_xml – volume: 194
  start-page: 1625
  year: 2001
  end-page: 1638
  ident: CR39
  article-title: Gene expression profiling of B cell chronic lymphocytic leukemia reveals a homogeneous phenotype related to memory B cells
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.194.11.1625
– volume: 119
  start-page: e161
  year: 2012
  end-page: e171
  ident: CR37
  article-title: Dynamic epigenetic enhancer signatures reveal key transcription factors associated with monocytic differentiation states
  publication-title: Blood
  doi: 10.1182/blood-2012-01-402453
– volume: 117
  start-page: 563
  year: 2011
  end-page: 574
  ident: CR32
  article-title: The lymph node microenvironment promotes B-cell receptor signaling, NF-κB activation, and tumor proliferation in chronic lymphocytic leukemia
  publication-title: Blood
  doi: 10.1182/blood-2010-05-284984
– volume: 8
  start-page: 2022
  year: 2013
  end-page: 2032
  ident: CR17
  article-title: Tagmentation-based whole-genome bisulfite sequencing
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2013.118
– volume: 47
  start-page: 1316
  year: 2015
  end-page: 1325
  ident: CR43
  article-title: DNA methylome analysis in Burkitt and follicular lymphomas identifies differentially methylated regions linked to somatic mutation and transcriptional control
  publication-title: Nat. Genet.
  doi: 10.1038/ng.3413
– volume: 9
  start-page: 687
  year: 2002
  end-page: 705
  ident: CR58
  article-title: Fast and accurate phylogeny reconstruction algorithms based on the minimum-evolution principle
  publication-title: J. Comput. Biol.
  doi: 10.1089/106652702761034136
– volume: 100
  start-page: 1410
  year: 2002
  end-page: 1416
  ident: CR51
  article-title: V mutation status, CD38 expression level, genomic aberrations, and survival in chronic lymphocytic leukemia
  publication-title: Blood
  doi: 10.1182/blood.V100.4.1410.h81602001410_1410_1416
– volume: 27
  start-page: 671
  year: 2013
  end-page: 679
  ident: CR60
  article-title: Role of early B-cell factor 1 (EBF1) in Hodgkin lymphoma
  publication-title: Leukemia
  doi: 10.1038/leu.2012.280
– volume: 151
  start-page: 25
  year: 2010
  end-page: 36
  ident: CR34
  article-title: Biological and clinical characterization of recurrent 14q deletions in CLL and other mature B-cell neoplasms
  publication-title: Br. J. Haematol.
  doi: 10.1111/j.1365-2141.2010.08299.x
– ident: CR54
– volume: 473
  start-page: 43
  year: 2011
  end-page: 49
  ident: CR20
  article-title: Mapping and analysis of chromatin state dynamics in nine human cell types
  publication-title: Nature
  doi: 10.1038/nature09906
– volume: 4
  start-page: 348
  year: 2014
  end-page: 361
  ident: CR13
  article-title: Evolution of DNA methylation is linked to genetic aberrations in chronic lymphocytic leukemia
  publication-title: Cancer Discov.
  doi: 10.1158/2159-8290.CD-13-0349
– volume: 124
  start-page: 42
  year: 2014
  end-page: 48
  ident: CR25
  article-title: Validation of ZAP-70 methylation and its relative significance in predicting outcome in chronic lymphocytic leukemia
  publication-title: Blood
  doi: 10.1182/blood-2014-02-555722
– volume: 3
  start-page: 581
  year: 2011
  end-page: 609
  ident: CR22
  article-title: Epigenomics of leukemia: from mechanisms to therapeutic applications
  publication-title: Epigenomics
  doi: 10.2217/epi.11.73
– volume: 13
  start-page: 497
  year: 2013
  end-page: 510
  ident: CR9
  article-title: Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host
  publication-title: Nat. Rev. Cancer
  doi: 10.1038/nrc3486
– volume: 20
  start-page: 400
  year: 2010
  end-page: 409
  ident: CR49
  article-title: Antigens in chronic lymphocytic leukemia—implications for cell origin and leukemogenesis
  publication-title: Semin. Cancer Biol.
  doi: 10.1016/j.semcancer.2010.09.004
– volume: 26
  start-page: 813
  year: 2014
  end-page: 825
  ident: CR14
  article-title: Locally disordered methylation forms the basis of intratumor methylome variation in chronic lymphocytic leukemia
  publication-title: Cancer Cell
  doi: 10.1016/j.ccell.2014.10.012
– volume: 118
  start-page: 3559
  year: 2011
  end-page: 3569
  ident: CR18
  article-title: DNA methyltransferase 1 and DNA methylation patterning contribute to germinal center B-cell differentiation
  publication-title: Blood
  doi: 10.1182/blood-2011-06-357996
– volume: 11
  start-page: 1138
  year: 2014
  end-page: 1140
  ident: CR56
  article-title: Comprehensive analysis of DNA methylation data with RnBeads
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.3115
– volume: 8
  start-page: 798
  year: 2014
  end-page: 806
  ident: CR57
  article-title: Epigenetic intratumor heterogeneity and clonal evolution in aggressive prostate cancer
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2014.06.053
– volume: 102
  start-page: 15545
  year: 2005
  end-page: 15550
  ident: CR59
  article-title: Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles
  publication-title: Proc. Natl. Acad. Sci. USA
– volume: 342
  start-page: 750
  year: 2013
  end-page: 752
  ident: CR5
  article-title: Extensive variation in chromatin states across humans
  publication-title: Science
  doi: 10.1126/science.1242510
– volume: 44
  start-page: 1236
  year: 2012
  end-page: 1242
  ident: CR10
  article-title: Epigenomic analysis detects widespread gene-body DNA hypomethylation in chronic lymphocytic leukemia
  publication-title: Nat. Genet.
  doi: 10.1038/ng.2443
– volume: 105
  start-page: 19643
  year: 2008
  end-page: 19648
  ident: CR50
  article-title: Tcl1 functions as a transcriptional regulator and is directly involved in the pathogenesis of CLL
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.0810965105
– volume: 475
  start-page: 101
  year: 2011
  end-page: 105
  ident: CR30
  article-title: Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia
  publication-title: Nature
  doi: 10.1038/nature10113
– volume: 517
  start-page: 321
  year: 2015
  end-page: 326
  ident: CR8
  article-title: Function and information content of DNA methylation
  publication-title: Nature
  doi: 10.1038/nature14192
– volume: 20
  start-page: 440
  year: 2010
  end-page: 446
  ident: CR23
  article-title: Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer
  publication-title: Genome Res.
  doi: 10.1101/gr.103606.109
– volume: 181
  start-page: 3364
  year: 2008
  end-page: 3372
  ident: CR26
  article-title: EBF1 is essential for B-lineage priming and establishment of a transcription factor network in common lymphoid progenitors
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.181.5.3364
– volume: 5
  start-page: e303
  year: 2015
  ident: CR24
  article-title: Genetic and epigenetic profiling of CLL disease progression reveals limited somatic evolution and suggests a relationship to memory-cell development
  publication-title: Blood Cancer J.
  doi: 10.1038/bcj.2015.14
– volume: 79
  start-page: 875
  year: 1994
  end-page: 884
  ident: CR44
  article-title: The helix-loop-helix gene is required for B cell formation
  publication-title: Cell
  doi: 10.1016/0092-8674(94)90076-0
– volume: 15
  start-page: 507
  year: 2014
  end-page: 522
  ident: CR7
  article-title: Identification of regulatory networks in HSCs and their immediate progeny via integrated proteome, transcriptome, and DNA methylome analysis
  publication-title: Cell Stem Cell
  doi: 10.1016/j.stem.2014.07.005
– volume: 188
  start-page: 1679
  year: 1998
  end-page: 1689
  ident: CR40
  article-title: Human immunoglobulin (Ig)M IgD peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.188.9.1679
– volume: 109
  start-page: 4424
  year: 2007
  end-page: 4431
  ident: CR33
  article-title: Reversible anergy of sIgM-mediated signaling in the two subsets of CLL defined by V -gene mutational status
  publication-title: Blood
  doi: 10.1182/blood-2006-11-056648
– volume: 26
  start-page: 589
  year: 2010
  end-page: 595
  ident: CR52
  article-title: Fast and accurate long-read alignment with Burrows-Wheeler transform
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btp698
– volume: 208
  start-page: 1135
  year: 2011
  end-page: 1149
  ident: CR27
  article-title: Ebf1 or Pax5 haploinsufficiency synergizes with STAT5 activation to initiate acute lymphoblastic leukemia
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20101947
– ident: CR2
– volume: 28
  start-page: 495
  year: 2010
  end-page: 501
  ident: CR61
  article-title: GREAT improves functional interpretation of -regulatory regions
  publication-title: Nat. Biotechnol.
  doi: 10.1038/nbt.1630
– volume: 500
  start-page: 477
  year: 2013
  end-page: 481
  ident: CR3
  article-title: Charting a dynamic DNA methylation landscape of the human genome
  publication-title: Nature
  doi: 10.1038/nature12433
– volume: 14
  start-page: 13
  year: 2001
  end-page: 20
  ident: CR46
  article-title: NFATc1 and NFATc2 together control both T and B cell activation and differentiation
  publication-title: Immunity
  doi: 10.1016/S1074-7613(01)00085-1
– volume: 209
  start-page: 2183
  year: 2012
  end-page: 2198
  ident: CR28
  article-title: Cellular origin and pathophysiology of chronic lymphocytic leukemia
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20120833
– volume: 42
  start-page: 3059
  year: 2014
  end-page: 3072
  ident: CR48
  article-title: c-Jun/c-Fos heterodimers regulate cellular genes via a newly identified class of methylated DNA sequence motifs
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkt1323
– volume: 120
  start-page: 4783
  year: 2012
  end-page: 4794
  ident: CR35
  article-title: High-resolution genomic profiling of chronic lymphocytic leukemia reveals new recurrent genomic alterations
  publication-title: Blood
  doi: 10.1182/blood-2012-04-423517
– volume: 4
  start-page: 1088
  year: 2014
  end-page: 1101
  ident: CR38
  article-title: Acquired initiating mutations in early hematopoietic cells of CLL patients
  publication-title: Cancer Discov.
  doi: 10.1158/2159-8290.CD-14-0104
– volume: 111
  start-page: 2685
  year: 2008
  end-page: 2692
  ident: CR41
  article-title: ZAP-70 enhances IgM signaling independent of its kinase activity in chronic lymphocytic leukemia
  publication-title: Blood
  doi: 10.1182/blood-2006-12-062265
– volume: 10
  start-page: 399
  year: 1999
  end-page: 408
  ident: CR47
  article-title: PU.1 and Spi-B are required for normal B cell receptor–mediated signal transduction
  publication-title: Immunity
  doi: 10.1016/S1074-7613(00)80040-0
– volume: 185
  start-page: 563
  year: 1997
  end-page: 571
  ident: CR16
  article-title: Germinal center founder cells display propensity for apoptosis before onset of somatic mutation
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.185.3.563
– volume: 22
  start-page: 425
  year: 2012
  end-page: 437
  ident: CR36
  article-title: Hotspot mutations in and define distinct epigenetic and biological subgroups of glioblastoma
  publication-title: Cancer Cell
  doi: 10.1016/j.ccr.2012.08.024
– volume: 23
  start-page: 2030
  year: 2013
  end-page: 2041
  ident: CR19
  article-title: DNA methylation profiling in human B cells reveals immune regulatory elements and epigenetic plasticity at Alu elements during B-cell activation
  publication-title: Genome Res.
  doi: 10.1101/gr.155473.113
– volume: 29
  start-page: 598
  year: 2015
  end-page: 605
  ident: CR11
  article-title: A B-cell epigenetic signature defines three biologic subgroups of chronic lymphocytic leukemia with clinical impact
  publication-title: Leukemia
  doi: 10.1038/leu.2014.252
– volume: 181
  start-page: 4590
  year: 2008
  end-page: 4602
  ident: CR45
  article-title: Early growth response genes regulate B cell development, proliferation, and immune response
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.181.7.4590
– volume: 507
  start-page: 455
  year: 2014
  end-page: 461
  ident: CR1
  article-title: An atlas of active enhancers across human cell types and tissues
  publication-title: Nature
  doi: 10.1038/nature12787
– volume: 345
  start-page: 943
  year: 2014
  end-page: 949
  ident: CR6
  article-title: Chromatin state dynamics during blood formation
  publication-title: Science
  doi: 10.1126/science.1256271
– volume: 42
  start-page: 637
  year: 2014
  end-page: 650
  ident: CR42
  article-title: The genome-wide molecular signature of transcription factors in leukemia
  publication-title: Exp. Hematol.
  doi: 10.1016/j.exphem.2014.04.012
– volume: 152
  start-page: 714
  year: 2013
  end-page: 726
  ident: CR31
  article-title: Evolution and impact of subclonal mutations in chronic lymphocytic leukemia
  publication-title: Cell
  doi: 10.1016/j.cell.2013.01.019
– volume: 24
  start-page: 212
  year: 2014
  end-page: 226
  ident: CR29
  article-title: Transcriptome characterization by RNA sequencing identifies a major molecular and clinical subdivision in chronic lymphocytic leukemia
  publication-title: Genome Res.
  doi: 10.1101/gr.152132.112
– volume: 1
  start-page: 177
  year: 2009
  end-page: 200
  ident: CR53
  article-title: Genome-wide DNA methylation profiling using Infinium assay
  publication-title: Epigenomics
  doi: 10.2217/epi.09.14
– volume: 111
  start-page: 16802
  year: 2014
  end-page: 16807
  ident: CR21
  article-title: Sample processing obscures cancer-specific alterations in leukemic transcriptomes
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.1413374111
– volume: 14
  start-page: 204
  year: 2013
  end-page: 220
  ident: CR4
  article-title: DNA methylation: roles in mammalian development
  publication-title: Nat. Rev. Genet.
– volume: 27
  start-page: 150
  year: 2013
  end-page: 158
  ident: CR12
  article-title: 450K-array analysis of chronic lymphocytic leukemia cells reveals global DNA methylation to be relatively stable over time and similar in resting and proliferative compartments
  publication-title: Leukemia
  doi: 10.1038/leu.2012.245
– volume: 47
  start-page: 746
  year: 2015
  end-page: 756
  ident: CR15
  article-title: Whole-genome fingerprint of the DNA methylome during human B cell differentiation
  publication-title: Nat. Genet.
  doi: 10.1038/ng.3291
– volume: 29
  start-page: 189
  year: 2013
  end-page: 196
  ident: CR55
  article-title: A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/bts680
– volume: 29
  start-page: 598
  year: 2015
  ident: BFng3488_CR11
  publication-title: Leukemia
  doi: 10.1038/leu.2014.252
– volume: 188
  start-page: 1679
  year: 1998
  ident: BFng3488_CR40
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.188.9.1679
– volume: 475
  start-page: 101
  year: 2011
  ident: BFng3488_CR30
  publication-title: Nature
  doi: 10.1038/nature10113
– volume: 111
  start-page: 2685
  year: 2008
  ident: BFng3488_CR41
  publication-title: Blood
  doi: 10.1182/blood-2006-12-062265
– volume: 9
  start-page: 687
  year: 2002
  ident: BFng3488_CR58
  publication-title: J. Comput. Biol.
  doi: 10.1089/106652702761034136
– volume: 102
  start-page: 15545
  year: 2005
  ident: BFng3488_CR59
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.0506580102
– volume: 15
  start-page: 507
  year: 2014
  ident: BFng3488_CR7
  publication-title: Cell Stem Cell
  doi: 10.1016/j.stem.2014.07.005
– volume: 473
  start-page: 43
  year: 2011
  ident: BFng3488_CR20
  publication-title: Nature
  doi: 10.1038/nature09906
– volume: 27
  start-page: 671
  year: 2013
  ident: BFng3488_CR60
  publication-title: Leukemia
  doi: 10.1038/leu.2012.280
– volume: 13
  start-page: 497
  year: 2013
  ident: BFng3488_CR9
  publication-title: Nat. Rev. Cancer
  doi: 10.1038/nrc3486
– volume: 4
  start-page: 1088
  year: 2014
  ident: BFng3488_CR38
  publication-title: Cancer Discov.
  doi: 10.1158/2159-8290.CD-14-0104
– volume: 5
  start-page: e303
  year: 2015
  ident: BFng3488_CR24
  publication-title: Blood Cancer J.
  doi: 10.1038/bcj.2015.14
– volume: 42
  start-page: 637
  year: 2014
  ident: BFng3488_CR42
  publication-title: Exp. Hematol.
  doi: 10.1016/j.exphem.2014.04.012
– volume: 20
  start-page: 400
  year: 2010
  ident: BFng3488_CR49
  publication-title: Semin. Cancer Biol.
  doi: 10.1016/j.semcancer.2010.09.004
– volume: 23
  start-page: 2030
  year: 2013
  ident: BFng3488_CR19
  publication-title: Genome Res.
  doi: 10.1101/gr.155473.113
– volume: 42
  start-page: 3059
  year: 2014
  ident: BFng3488_CR48
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkt1323
– volume: 500
  start-page: 477
  year: 2013
  ident: BFng3488_CR3
  publication-title: Nature
  doi: 10.1038/nature12433
– volume: 117
  start-page: 563
  year: 2011
  ident: BFng3488_CR32
  publication-title: Blood
  doi: 10.1182/blood-2010-05-284984
– volume: 8
  start-page: 2022
  year: 2013
  ident: BFng3488_CR17
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2013.118
– volume: 27
  start-page: 150
  year: 2013
  ident: BFng3488_CR12
  publication-title: Leukemia
  doi: 10.1038/leu.2012.245
– volume: 24
  start-page: 212
  year: 2014
  ident: BFng3488_CR29
  publication-title: Genome Res.
  doi: 10.1101/gr.152132.112
– volume: 47
  start-page: 1316
  year: 2015
  ident: BFng3488_CR43
  publication-title: Nat. Genet.
  doi: 10.1038/ng.3413
– volume: 29
  start-page: 189
  year: 2013
  ident: BFng3488_CR55
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/bts680
– volume: 120
  start-page: 4783
  year: 2012
  ident: BFng3488_CR35
  publication-title: Blood
  doi: 10.1182/blood-2012-04-423517
– volume: 181
  start-page: 4590
  year: 2008
  ident: BFng3488_CR45
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.181.7.4590
– volume: 185
  start-page: 563
  year: 1997
  ident: BFng3488_CR16
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.185.3.563
– volume: 3
  start-page: 581
  year: 2011
  ident: BFng3488_CR22
  publication-title: Epigenomics
  doi: 10.2217/epi.11.73
– volume: 8
  start-page: 798
  year: 2014
  ident: BFng3488_CR57
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2014.06.053
– ident: BFng3488_CR54
  doi: 10.1126/science.1105136
– volume: 345
  start-page: 943
  year: 2014
  ident: BFng3488_CR6
  publication-title: Science
  doi: 10.1126/science.1256271
– volume: 209
  start-page: 2183
  year: 2012
  ident: BFng3488_CR28
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20120833
– ident: BFng3488_CR2
– volume: 26
  start-page: 589
  year: 2010
  ident: BFng3488_CR52
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btp698
– volume: 181
  start-page: 3364
  year: 2008
  ident: BFng3488_CR26
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.181.5.3364
– volume: 22
  start-page: 425
  year: 2012
  ident: BFng3488_CR36
  publication-title: Cancer Cell
  doi: 10.1016/j.ccr.2012.08.024
– volume: 111
  start-page: 16802
  year: 2014
  ident: BFng3488_CR21
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.1413374111
– volume: 507
  start-page: 455
  year: 2014
  ident: BFng3488_CR1
  publication-title: Nature
  doi: 10.1038/nature12787
– volume: 10
  start-page: 399
  year: 1999
  ident: BFng3488_CR47
  publication-title: Immunity
  doi: 10.1016/S1074-7613(00)80040-0
– volume: 342
  start-page: 750
  year: 2013
  ident: BFng3488_CR5
  publication-title: Science
  doi: 10.1126/science.1242510
– volume: 47
  start-page: 746
  year: 2015
  ident: BFng3488_CR15
  publication-title: Nat. Genet.
  doi: 10.1038/ng.3291
– volume: 20
  start-page: 440
  year: 2010
  ident: BFng3488_CR23
  publication-title: Genome Res.
  doi: 10.1101/gr.103606.109
– volume: 517
  start-page: 321
  year: 2015
  ident: BFng3488_CR8
  publication-title: Nature
  doi: 10.1038/nature14192
– volume: 44
  start-page: 1236
  year: 2012
  ident: BFng3488_CR10
  publication-title: Nat. Genet.
  doi: 10.1038/ng.2443
– volume: 118
  start-page: 3559
  year: 2011
  ident: BFng3488_CR18
  publication-title: Blood
  doi: 10.1182/blood-2011-06-357996
– volume: 124
  start-page: 42
  year: 2014
  ident: BFng3488_CR25
  publication-title: Blood
  doi: 10.1182/blood-2014-02-555722
– volume: 105
  start-page: 19643
  year: 2008
  ident: BFng3488_CR50
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.0810965105
– volume: 1
  start-page: 177
  year: 2009
  ident: BFng3488_CR53
  publication-title: Epigenomics
  doi: 10.2217/epi.09.14
– volume: 11
  start-page: 1138
  year: 2014
  ident: BFng3488_CR56
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.3115
– volume: 28
  start-page: 495
  year: 2010
  ident: BFng3488_CR61
  publication-title: Nat. Biotechnol.
  doi: 10.1038/nbt.1630
– volume: 4
  start-page: 348
  year: 2014
  ident: BFng3488_CR13
  publication-title: Cancer Discov.
  doi: 10.1158/2159-8290.CD-13-0349
– volume: 208
  start-page: 1135
  year: 2011
  ident: BFng3488_CR27
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20101947
– volume: 194
  start-page: 1625
  year: 2001
  ident: BFng3488_CR39
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.194.11.1625
– volume: 79
  start-page: 875
  year: 1994
  ident: BFng3488_CR44
  publication-title: Cell
  doi: 10.1016/0092-8674(94)90076-0
– volume: 119
  start-page: e161
  year: 2012
  ident: BFng3488_CR37
  publication-title: Blood
  doi: 10.1182/blood-2012-01-402453
– volume: 100
  start-page: 1410
  year: 2002
  ident: BFng3488_CR51
  publication-title: Blood
  doi: 10.1182/blood.V100.4.1410.h81602001410_1410_1416
– volume: 109
  start-page: 4424
  year: 2007
  ident: BFng3488_CR33
  publication-title: Blood
  doi: 10.1182/blood-2006-11-056648
– volume: 26
  start-page: 813
  year: 2014
  ident: BFng3488_CR14
  publication-title: Cancer Cell
  doi: 10.1016/j.ccell.2014.10.012
– volume: 152
  start-page: 714
  year: 2013
  ident: BFng3488_CR31
  publication-title: Cell
  doi: 10.1016/j.cell.2013.01.019
– volume: 14
  start-page: 204
  year: 2013
  ident: BFng3488_CR4
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg3354
– volume: 151
  start-page: 25
  year: 2010
  ident: BFng3488_CR34
  publication-title: Br. J. Haematol.
  doi: 10.1111/j.1365-2141.2010.08299.x
– volume: 14
  start-page: 13
  year: 2001
  ident: BFng3488_CR46
  publication-title: Immunity
  doi: 10.1016/S1074-7613(01)00085-1
– reference: 11733577 - J Exp Med. 2001 Dec 3;194(11):1625-38
– reference: 24670763 - Nature. 2014 Mar 27;507(7493):455-61
– reference: 20080505 - Bioinformatics. 2010 Mar 1;26(5):589-95
– reference: 23174882 - Leukemia. 2013 Mar;27(3):671-9
– reference: 18714008 - J Immunol. 2008 Sep 1;181(5):3364-72
– reference: 20863893 - Semin Cancer Biol. 2010 Dec;20(6):400-9
– reference: 21606506 - J Exp Med. 2011 Jun 6;208(6):1135-49
– reference: 12149225 - Blood. 2002 Aug 15;100(4):1410-6
– reference: 8001124 - Cell. 1994 Dec 2;79(5):875-84
– reference: 10229183 - Immunity. 1999 Apr;10(4):399-408
– reference: 23064414 - Nat Genet. 2012 Nov;44(11):1236-42
– reference: 21441907 - Nature. 2011 May 5;473(7345):43-9
– reference: 22550342 - Blood. 2012 Jun 14;119(24):e161-71
– reference: 21642962 - Nature. 2011 Jun 05;475(7354):101-5
– reference: 25151957 - Leukemia. 2015 Mar;29(3):598-605
– reference: 24136358 - Science. 2013 Nov 8;342(6159):750-2
– reference: 26053498 - Nat Genet. 2015 Jul;47(7):746-56
– reference: 15499007 - Science. 2004 Oct 22;306(5696):636-40
– reference: 24013550 - Genome Res. 2013 Dec;23(12):2030-41
– reference: 23415222 - Cell. 2013 Feb 14;152(4):714-26
– reference: 24071908 - Nat Protoc. 2013 Oct;8(10):2022-32
– reference: 25592537 - Nature. 2015 Jan 15;517(7534):321-6
– reference: 23091163 - J Exp Med. 2012 Nov 19;209(12):2183-98
– reference: 25490447 - Cancer Cell. 2014 Dec 8;26(6):813-25
– reference: 25262207 - Nat Methods. 2014 Nov;11(11):1138-40
– reference: 9053456 - J Exp Med. 1997 Feb 3;185(3):563-71
– reference: 26437030 - Nat Genet. 2015 Nov;47(11):1316-25
– reference: 22922567 - Leukemia. 2013 Jan;27(1):150-8
– reference: 25693563 - Nature. 2015 Feb 19;518(7539):317-30
– reference: 23760024 - Nat Rev Cancer. 2013 Jul;13(7):497-510
– reference: 23175756 - Bioinformatics. 2013 Jan 15;29(2):189-96
– reference: 24371273 - Nucleic Acids Res. 2014 Mar;42(5):3059-72
– reference: 25103404 - Science. 2014 Aug 22;345(6199):943-9
– reference: 21828137 - Blood. 2011 Sep 29;118(13):3559-69
– reference: 19064921 - Proc Natl Acad Sci U S A. 2008 Dec 16;105(50):19643-8
– reference: 20436461 - Nat Biotechnol. 2010 May;28(5):495-501
– reference: 25860294 - Blood Cancer J. 2015 Apr 10;5:e303
– reference: 12487758 - J Comput Biol. 2002;9(5):687-705
– reference: 24920063 - Cancer Discov. 2014 Sep;4(9):1088-101
– reference: 20940416 - Blood. 2011 Jan 13;117(2):563-74
– reference: 22126248 - Epigenomics. 2011 Oct;3(5):581-609
– reference: 24868078 - Blood. 2014 Jul 3;124(1):42-8
– reference: 22122642 - Epigenomics. 2009 Oct;1(1):177-200
– reference: 23400093 - Nat Rev Genet. 2013 Mar;14(3):204-20
– reference: 25385641 - Proc Natl Acad Sci U S A. 2014 Nov 25;111(47):16802-7
– reference: 24265505 - Genome Res. 2014 Feb;24(2):212-26
– reference: 25066126 - Cell Rep. 2014 Aug 7;8(3):798-806
– reference: 24814246 - Exp Hematol. 2014 Aug;42(8):637-50
– reference: 23047824 - Blood. 2012 Dec 6;120(24):4783-94
– reference: 18802061 - J Immunol. 2008 Oct 1;181(7):4590-602
– reference: 17255355 - Blood. 2007 May 15;109(10):4424-31
– reference: 20649559 - Br J Haematol. 2010 Oct;151(1):25-36
– reference: 24356097 - Cancer Discov. 2014 Mar;4(3):348-61
– reference: 23079654 - Cancer Cell. 2012 Oct 16;22(4):425-37
– reference: 25158935 - Cell Stem Cell. 2014 Oct 2;15(4):507-22
– reference: 23925113 - Nature. 2013 Aug 22;500(7463):477-81
– reference: 11163226 - Immunity. 2001 Jan;14(1):13-20
– reference: 20219944 - Genome Res. 2010 Apr;20(4):440-6
– reference: 9802980 - J Exp Med. 1998 Nov 2;188(9):1679-89
– reference: 16199517 - Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50
– reference: 18048647 - Blood. 2008 Mar 1;111(5):2685-92
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Snippet Christoph Plass, Christopher Oakes and colleagues study genome-wide DNA methylation dynamics during B cell maturation and the pathogenic role of transcription...
Charting differences between tumors and normal tissue is a mainstay of cancer research. However, clonal tumor expansion from complex normal tissue...
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StartPage 253
SubjectTerms 13/1
13/106
38/91
45/22
45/23
45/90
631/208/177
692/699/67/1990/283/1895
Adult
Aged
Aged, 80 and over
Agriculture
Animal Genetics and Genomics
B cells
B-Lymphocytes - immunology
B-Lymphocytes - metabolism
Binding Sites
Biomedicine
Cancer
Cancer Research
Chronic lymphocytic leukemia
Consortia
CpG Islands - genetics
Deoxyribonucleic acid
Development and progression
Developmental stages
DNA
DNA methylation
DNA Methylation - genetics
Epigenesis, Genetic
Epigenetic inheritance
Epigenetics
Female
Gene expression
Gene Expression Regulation, Leukemic
Gene Expression Regulation, Neoplastic
Gene Function
Genetic aspects
Genomes
Growth
Health aspects
Human Genetics
Humans
Leukemia
Leukemia, Lymphocytic, Chronic, B-Cell - genetics
Leukemia, Lymphocytic, Chronic, B-Cell - immunology
Leukemia, Lymphocytic, Chronic, B-Cell - pathology
Male
Medical research
Middle Aged
Neoplasm Proteins - biosynthesis
Neoplasm Proteins - genetics
Phenotype
Promoter Regions, Genetic
Software
Transcription factors
Tumors
Title DNA methylation dynamics during B cell maturation underlie a continuum of disease phenotypes in chronic lymphocytic leukemia
URI https://link.springer.com/article/10.1038/ng.3488
https://www.ncbi.nlm.nih.gov/pubmed/26780610
https://www.proquest.com/docview/1770389453
https://www.proquest.com/docview/1768167104
https://www.proquest.com/docview/1808740193
https://pubmed.ncbi.nlm.nih.gov/PMC4963005
Volume 48
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