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Paradoxical role of Id proteins in regulating tumorigenic potential of lymphoid cells |
Sumedha Roy(), Yuan Zhuang |
Department of Immunology, Duke University Medical Center, Durham, NC 27710, USA |
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Abstract A family of transcription factors known as Id proteins, or inhibitor of DNA binding and differentiation, is capable of regulating cell proliferation, survival and differentiation, and is often upregulated in multiple types of tumors. Due to their ability to promote self-renewal, Id proteins have been considered as oncogenes, and potential therapeutic targets in cancer models. On the contrary, certain Id proteins are reported to act as tumor suppressors in the development of Burkitt’s lymphoma in humans, and hepatosplenic and innate-like T cell lymphomas in mice. The contexts and mechanisms by which Id proteins can serve in such contradictory roles to determine tumor outcomes are still not well understood. In this review, we explore the roles of Id proteins in lymphocyte development and tumorigenesis, particularly with respect to inhibition of their canonical DNA binding partners known as E proteins. Transcriptional regulation by E proteins, and their antagonism by Id proteins, act as gatekeepers to ensure appropriate lymphocyte development at key checkpoints. We re-examine the derailment of these regulatory mechanisms in lymphocytes that facilitate tumor development. These mechanistic insights can allow better appreciation of the context-dependent roles of Id proteins in cancers and improve considerations for therapy.
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Keywords
Id proteins
lymphoma
leukemia
T cells
B cells
tumor suppressor
oncogene
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Corresponding Author(s):
Sumedha Roy
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Just Accepted Date: 09 July 2018
Online First Date: 25 July 2018
Issue Date: 03 September 2018
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|
1 |
Norton JD, Deed RW, Craggs G, Sablitzky F. Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol 1998; 8(2): 58–65
pmid: 9695810
|
2 |
Lasorella A, Uo T, Iavarone A. Id proteins at the cross-road of development and cancer. Oncogene 2001; 20(58): 8326–8333
https://doi.org/10.1038/sj.onc.1205093
pmid: 11840325
|
3 |
Sikder HA, Devlin MK, Dunlap S, Ryu B, Alani RM. Id proteins in cell growth and tumorigenesis. Cancer Cell 2003; 3(6): 525–530
https://doi.org/10.1016/S1535-6108(03)00141-7
pmid: 12842081
|
4 |
Perk J, Iavarone A, Benezra R. Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer 2005; 5(8): 603–614
https://doi.org/10.1038/nrc1673
pmid: 16034366
|
5 |
Lasorella A, Benezra R, Iavarone A. The ID proteins: master regulators of cancer stem cells and tumour aggressiveness. Nat Rev Cancer 2014; 14(2): 77–91
https://doi.org/10.1038/nrc3638
pmid: 24442143
|
6 |
Hasskarl J, Münger K. Id proteins—tumor markers or oncogenes? Cancer Biol Ther 2002; 1(2): 91–96
https://doi.org/10.4161/cbt.50
pmid: 12170780
|
7 |
Roschger C, Cabrele C. The Id-protein family in developmental and cancer-associated pathways. Cell Commun Signal 2017; 15(1): 7
https://doi.org/10.1186/s12964-016-0161-y
pmid: 28122577
|
8 |
Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990; 61(1): 49–59
https://doi.org/10.1016/0092-8674(90)90214-Y
pmid: 2156629
|
9 |
Langlands K, Yin X, Anand G, Prochownik EV. Differential interactions of Id proteins with basic-helix-loop-helix transcription factors. J Biol Chem 1997; 272(32): 19785–19793
https://doi.org/10.1074/jbc.272.32.19785
pmid: 9242638
|
10 |
Israel MA, Hernandez MC, Florio M, Andres-Barquin PJ, Mantani A, Carter JH, Julin CM. Id gene expression as a key mediator of tumor cell biology. Cancer Res 1999; 59(7 Suppl): 1726s–1730s
pmid: 10197587
|
11 |
Norton JD, Atherton GT. Coupling of cell growth control and apoptosis functions of Id proteins. Mol Cell Biol 1998; 18(4): 2371–2381
https://doi.org/10.1128/MCB.18.4.2371
pmid: 9528806
|
12 |
Wong YC, Wang X, Ling MT. Id-1 expression and cell survival. Apoptosis 2004; 9(3): 279–289
https://doi.org/10.1023/B:APPT.0000025804.25396.79
pmid: 15258459
|
13 |
Engel I, Murre C. E2A proteins enforce a proliferation checkpoint in developing thymocytes. EMBO J 2004; 23(1): 202–211
https://doi.org/10.1038/sj.emboj.7600017
pmid: 14685278
|
14 |
Slattery C, Ryan MP, McMorrow T. E2A proteins: regulators of cell phenotype in normal physiology and disease. Int J Biochem Cell Biol 2008; 40(8): 1431–1436
https://doi.org/10.1016/j.biocel.2007.05.014
pmid: 17604208
|
15 |
Tang J, Gordon GM, Nickoloff BJ, Foreman KE. The helix-loop-helix protein Id-1 delays onset of replicative senescence in human endothelial cells. Lab Invest 2002; 82(8): 1073–1079
https://doi.org/10.1097/01.LAB.0000022223.65962.3A
pmid: 12177246
|
16 |
Neuhold LA, Wold B. HLH forced dimers: tethering MyoD to E47 generates a dominant positive myogenic factor insulated from negative regulation by Id. Cell 1993; 74(6): 1033–1042
https://doi.org/10.1016/0092-8674(93)90725-6
pmid: 7691411
|
17 |
Deed RW, Armitage S, Norton JD. Nuclear localization and regulation of Id protein through an E protein-mediated chaperone mechanism. J Biol Chem 1996; 271(39): 23603–23606
https://doi.org/10.1074/jbc.271.39.23603
pmid: 8798572
|
18 |
Zhuang Y, Soriano P, Weintraub H. The helix-loop-helix gene E2A is required for B cell formation. Cell 1994; 79(5): 875–884
https://doi.org/10.1016/0092-8674(94)90076-0
pmid: 8001124
|
19 |
Bain G, Maandag EC, Izon DJ, Amsen D, Kruisbeek AM, Weintraub BC, Krop I, Schlissel MS, Feeney AJ, van Roon M, van der Valk M, te Riele HPJ, Berns A, Murre C. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 1994; 79(5): 885–892
https://doi.org/10.1016/0092-8674(94)90077-9
pmid: 8001125
|
20 |
Engel I, Johns C, Bain G, Rivera RR, Murre C. Early thymocyte development is regulated by modulation of E2A protein activity. J Exp Med 2001; 194(6): 733–745
https://doi.org/10.1084/jem.194.6.733
pmid: 11560990
|
21 |
Greenbaum S, Zhuang Y. Regulation of early lymphocyte development by E2A family proteins. Semin Immunol 2002; 14(6): 405–414
https://doi.org/10.1016/S1044532302000751
pmid: 12457613
|
22 |
Zhuang Y, Jackson A, Pan L, Shen K, Dai M. Regulation of E2A gene expression in B-lymphocyte development. Mol Immunol 2004; 40(16): 1165–1177
https://doi.org/10.1016/j.molimm.2003.11.031
pmid: 15104122
|
23 |
Greenbaum S, Zhuang Y. Identification of E2A target genes in B lymphocyte development by using a gene tagging-based chromatin immunoprecipitation system. Proc Natl Acad Sci USA 2002; 99(23): 15030–15035
https://doi.org/10.1073/pnas.232299999
pmid: 12415115
|
24 |
Lin YC, Jhunjhunwala S, Benner C, Heinz S, Welinder E, Mansson R, Sigvardsson M, Hagman J, Espinoza CA, Dutkowski J, Ideker T, Glass CK, Murre C. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat Immunol 2010; 11(7): 635–643
https://doi.org/10.1038/ni.1891
pmid: 20543837
|
25 |
Murre C. Helix-loop-helix proteins and lymphocyte development. Nat Immunol 2005; 6(11): 1079–1086
https://doi.org/10.1038/ni1260
pmid: 16239924
|
26 |
Miyazaki K, Miyazaki M, Murre C. The establishment of B versus T cell identity. Trends Immunol 2014; 35(5): 205–210
https://doi.org/10.1016/j.it.2014.02.009
pmid: 24679436
|
27 |
Kwon K, Hutter C, Sun Q, Bilic I, Cobaleda C, Malin S, Busslinger M. Instructive role of the transcription factor E2A in early B lymphopoiesis and germinal center B cell development. Immunity 2008; 28(6): 751–762
https://doi.org/10.1016/j.immuni.2008.04.014
pmid: 18538592
|
28 |
Herblot S, Aplan PD, Hoang T. Gradient of E2A activity in B-cell development. Mol Cell Biol 2002; 22(3): 886–900
https://doi.org/10.1128/MCB.22.3.886-900.2002
pmid: 11784864
|
29 |
Kee BL, Rivera RR, Murre C. Id3 inhibits B lymphocyte progenitor growth and survival in response to TGF-β. Nat Immunol 2001; 2(3): 242–247
https://doi.org/10.1038/85303
pmid: 11224524
|
30 |
Chen S, Miyazaki M, Chandra V, Fisch KM, Chang AN, Murre C. Id3 orchestrates germinal center b cell development. Mol Cell Biol 2016; 36(20): 2543–2552
https://doi.org/10.1128/MCB.00150-16
pmid: 27457619
|
31 |
Boxer LM, Dang CV. Translocations involving c-myc and c-myc function. Oncogene 2001; 20(40): 5595–5610
https://doi.org/10.1038/sj.onc.1204595
pmid: 11607812
|
32 |
Miles RR, Raphael M, McCarthy K, Wotherspoon A, Lones MA, Terrier-Lacombe MJ, Patte C, Gerrard M, Auperin A, Sposto R, Davenport V, Cairo MS, Perkins SL; SFOP/LMB96/CCG5961/UKCCSG/NHL 9600 Study Group. Pediatric diffuse large B-cell lymphoma demonstrates a high proliferation index, frequent c-Myc protein expression, and a high incidence of germinal center subtype: report of the French-American-British (FAB) international study group. Pediatr Blood Cancer 2008; 51(3): 369–374
https://doi.org/10.1002/pbc.21619
pmid: 18493992
|
33 |
Love C, Sun Z, Jima D, Li G, Zhang J, Miles R, Richards KL, Dunphy CH, Choi WW, Srivastava G, Lugar PL, Rizzieri DA, Lagoo AS, Bernal-Mizrachi L, Mann KP, Flowers CR, Naresh KN, Evens AM, Chadburn A, Gordon LI, Czader MB, Gill JI, Hsi ED, Greenough A, Moffitt AB, McKinney M, Banerjee A, Grubor V, Levy S, Dunson DB, Dave SS. The genetic landscape of mutations in Burkitt lymphoma. Nat Genet 2012; 44(12): 1321–1325
https://doi.org/10.1038/ng.2468
pmid: 23143597
|
34 |
Richter J, Schlesner M, Hoffmann S, Kreuz M, Leich E, Burkhardt B, Rosolowski M, Ammerpohl O, Wagener R, Bernhart SH, Lenze D, Szczepanowski M, Paulsen M, Lipinski S, Russell RB, Adam-Klages S, Apic G, Claviez A, Hasenclever D, Hovestadt V, Hornig N, Korbel JO, Kube D, Langenberger D, Lawerenz C, Lisfeld J, Meyer K, Picelli S, Pischimarov J, Radlwimmer B, Rausch T, Rohde M, Schilhabel M, Scholtysik R, Spang R, Trautmann H, Zenz T, Borkhardt A, Drexler HG, Möller P, MacLeod RA, Pott C, Schreiber S, Trümper L, Loeffler M, Stadler PF, Lichter P, Eils R, Küppers R, Hummel M, Klapper W, Rosenstiel P, Rosenwald A, Brors B, Siebert R; ICGC MMML-Seq Project. Recurrent mutation of the ID3 gene in Burkitt lymphoma identified by integrated genome, exome and transcriptome sequencing. Nat Genet 2012; 44(12): 1316–1320
https://doi.org/10.1038/ng.2469
pmid: 23143595
|
35 |
Schmitz R, Young RM, Ceribelli M, Jhavar S, Xiao W, Zhang M, Wright G, Shaffer AL, Hodson DJ, Buras E, Liu X, Powell J, Yang Y, Xu W, Zhao H, Kohlhammer H, Rosenwald A, Kluin P, Müller-Hermelink HK, Ott G, Gascoyne RD, Connors JM, Rimsza LM, Campo E, Jaffe ES, Delabie J, Smeland EB, Ogwang MD, Reynolds SJ, Fisher RI, Braziel RM, Tubbs RR, Cook JR, Weisenburger DD, Chan WC, Pittaluga S, Wilson W, Waldmann TA, Rowe M, Mbulaiteye SM, Rickinson AB, Staudt LM. Burkitt lymphoma pathogenesis and therapeutic targets from structural and functional genomics. Nature 2012; 490(7418): 116–120
https://doi.org/10.1038/nature11378
pmid: 22885699
|
36 |
Havelange V, Pepermans X, Ameye G, Théate I, Callet-Bauchu E, Barin C, Penther D, Lippert E, Michaux L, Mugneret F, Dastugue N, Raphaël M, Vikkula M, Poirel HA. Genetic differences between paediatric and adult Burkitt lymphomas. Br J Haematol 2016; 173(1): 137–144
https://doi.org/10.1111/bjh.13925
pmid: 26887776
|
37 |
Cato MH, Chintalapati SK, Yau IW, Omori SA, Rickert RC. Cyclin D3 is selectively required for proliferative expansion of germinal center B cells. Mol Cell Biol 2011; 31(1): 127–137
https://doi.org/10.1128/MCB.00650-10
pmid: 20956554
|
38 |
Peled JU, Yu JJ, Venkatesh J, Bi E, Ding BB, Krupski-Downs M, Shaknovich R, Sicinski P, Diamond B, Scharff MD, Ye BH. Requirement for cyclin D3 in germinal center formation and function. Cell Res 2010; 20(6): 631–646
https://doi.org/10.1038/cr.2010.55
pmid: 20404856
|
39 |
Rohde M, Bonn BR, Zimmermann M, Lange J, Möricke A, Klapper W, Oschlies I, Szczepanowski M, Nagel I, Schrappe M; MMML-MYC-SYS Project; ICGC MMML-Seq Project, Loeffler M, Siebert R, Reiter A, Burkhardt B. Relevance of ID3-TCF3-CCND3 pathway mutations in pediatric aggressive B-cell lymphoma treated according to the non-Hodgkin Lymphoma Berlin-Frankfurt-Münster protocols. Haematologica 2017; 102(6): 1091–1098
https://doi.org/10.3324/haematol.2016.156885
pmid: 28209658
|
40 |
Kee BLE. E and ID proteins branch out. Nat Rev Immunol 2009; 9(3): 175–184
https://doi.org/10.1038/nri2507
pmid: 19240756
|
41 |
Roschke V, Kopantzev E, Dertzbaugh M, Rudikoff S. Chromosomal translocations deregulating c-myc are associated with normal immune responses. Oncogene 1997; 14(25): 3011–3016
https://doi.org/10.1038/sj.onc.1201156
pmid: 9223664
|
42 |
Nepal RM, Zaheen A, Basit W, Li L, Berger SA, Martin A. AID and RAG1 do not contribute to lymphomagenesis in Emu c-myc transgenic mice. Oncogene 2008; 27(34): 4752–4756
https://doi.org/10.1038/onc.2008.111
pmid: 18408759
|
43 |
Scholtysik R, Kreuz M, Klapper W, Burkhardt B, Feller AC, Hummel M, Loeffler M, Rosolowski M, Schwaenen C, Spang R, Stein H, Thorns C, Trümper L, Vater I, Wessendorf S, Zenz T, Siebert R, Küppers R; Molecular Mechanisms in Malignant Lymphomas Network Project of Deutsche Krebshilfe. Detection of genomic aberrations in molecularly defined Burkitt’s lymphoma by array-based, high resolution, single nucleotide polymorphism analysis. Haematologica 2010; 95(12): 2047–2055
https://doi.org/10.3324/haematol.2010.026831
pmid: 20823134
|
44 |
Salaverria I, Martin-Guerrero I, Wagener R, Kreuz M, Kohler CW, Richter J, Pienkowska-Grela B, Adam P, Burkhardt B, Claviez A, Damm-Welk C, Drexler HG, Hummel M, Jaffe ES, Küppers R, Lefebvre C, Lisfeld J, Löffler M, Macleod RA, Nagel I, Oschlies I, Rosolowski M, Russell RB, Rymkiewicz G, Schindler D, Schlesner M, Scholtysik R, Schwaenen C, Spang R, Szczepanowski M, Trümper L, Vater I, Wessendorf S, Klapper W, Siebert R; Molecular Mechanisms in Malignant Lymphoma Network Project; Berlin-Frankfurt-Münster Non-Hodgkin Lymphoma Group. A recurrent 11q aberration pattern characterizes a subset of MYC-negative high-grade B-cell lymphomas resembling Burkitt lymphoma. Blood 2014; 123(8): 1187–1198
https://doi.org/10.1182/blood-2013-06-507996
pmid: 24398325
|
45 |
Campo E. New pathogenic mechanisms in Burkitt lymphoma. Nat Genet 2012; 44(12): 1288–1289
https://doi.org/10.1038/ng.2476
pmid: 23192177
|
46 |
Forshell LP, Li Y, Forshell TZ, Rudelius M, Nilsson L, Keller U, Nilsson J. The direct Myc target Pim3 cooperates with other Pim kinases in supporting viability of Myc-induced B-cell lymphomas. Oncotarget 2011; 2(6): 448–460
https://doi.org/10.18632/oncotarget.283
pmid: 21646687
|
47 |
Murphy DJ, Swigart LB, Israel MA, Evan GI. Id2 is dispensable for Myc-induced epidermal neoplasia. Mol Cell Biol 2004; 24(5): 2083–2090
https://doi.org/10.1128/MCB.24.5.2083-2090.2004
pmid: 14966287
|
48 |
Gao XZ, Zhao WG, Wang GN, Cui MY, Zhang YR, Li WC. Inhibitor of DNA binding 4 functions as a tumor suppressor and is targetable by 5-aza-2′-deoxycytosine with potential therapeutic significance in Burkitt’s lymphoma. Mol Med Rep 2016; 13(2): 1269–1274
https://doi.org/10.3892/mmr.2015.4640
pmid: 26648013
|
49 |
Spender LC, Inman GJ. TGF-β induces growth arrest in Burkitt lymphoma cells via transcriptional repression of E2F-1. J Biol Chem 2009; 284(3): 1435–1442
https://doi.org/10.1074/jbc.M808080200
pmid: 19022773
|
50 |
Bakkebø M, Huse K, Hilden VI, Smeland EB, Oksvold MP. TGF-β-induced growth inhibition in B-cell lymphoma correlates with Smad1/5 signalling and constitutively active p38 MAPK. BMC Immunol 2010; 11(1): 57
https://doi.org/10.1186/1471-2172-11-57
pmid: 21092277
|
51 |
Reddy A, Zhang J, Davis NS, Moffitt AB, Love CL, Waldrop A, Leppa S, Pasanen A, Meriranta L, Karjalainen-Lindsberg ML, Norgaard P, Pedersen M, Gang AO, Hogdall E, Heavican TB, Lone W, Iqbal J, Qin Q, Li G, Kim SY, Healy J, Richards KL, Fedoriw Y, Bernal-Mizrachi L, Koff JL, Staton AD, Flowers CR, Paltiel O, Goldschmidt N, Calaminici M, Clear A, Gribben J, Nguyen E, Czader MB, Ondrejka SL, Collie A, Hsi ED, Tse E, Au-Yeung RKH, Kwong YL, Srivastava G, Choi WWL, Evens AM, Pilichowska M, Sengar M, Reddy N, Li S, Chadburn A, Gordon LI, Jaffe ES, Levy S, Rempel R, Tzeng T, Happ LE, Dave T, Rajagopalan D, Datta J, Dunson DB, and Dave SS. Genetic and functional drivers of diffuse large B cell lymphoma. Cell 2017; 171(2): p. 481–494e15
|
52 |
Dubois S, Viailly PJ, Mareschal S, Bohers E, Bertrand P, Ruminy P, Maingonnat C, Jais JP, Peyrouze P, Figeac M, Molina TJ, Desmots F, Fest T, Haioun C, Lamy T, Copie-Bergman C, Brière J, Petrella T, Canioni D, Fabiani B, Coiffier B, Delarue R, Peyrade F, Bosly A, André M, Ketterer N, Salles G, Tilly H, Leroy K, Jardin F. Next-generation sequencing in diffuse large B-cell lymphoma highlights molecular divergence and therapeutic opportunities: a LYSA study. Clin Cancer Res 2016; 22(12): 2919–2928
https://doi.org/10.1158/1078-0432.CCR-15-2305
pmid: 26819451
|
53 |
Momose S, Weißbach S, Pischimarov J, Nedeva T, Bach E, Rudelius M, Geissinger E, Staiger AM, Ott G, Rosenwald A. The diagnostic gray zone between Burkitt lymphoma and diffuse large B-cell lymphoma is also a gray zone of the mutational spectrum. Leukemia 2015; 29(8): 1789–1791
https://doi.org/10.1038/leu.2015.34
pmid: 25673238
|
54 |
Gebauer N, Bernard V, Feller AC, Merz H. ID3 mutations are recurrent events in double-hit B-cell lymphomas. Anticancer Res 2013; 33(11): 4771–4778
pmid: 24222112
|
55 |
Dave SS, Fu K, Wright GW, Lam LT, Kluin P, Boerma EJ, Greiner TC, Weisenburger DD, Rosenwald A, Ott G, Müller-Hermelink HK, Gascoyne RD, Delabie J, Rimsza LM, Braziel RM, Grogan TM, Campo E, Jaffe ES, Dave BJ, Sanger W, Bast M, Vose JM, Armitage JO, Connors JM, Smeland EB, Kvaloy S, Holte H, Fisher RI, Miller TP, Montserrat E, Wilson WH, Bahl M, Zhao H, Yang L, Powell J, Simon R, Chan WC, Staudt LM; Lymphoma/Leukemia Molecular Profiling Project. Molecular diagnosis of Burkitt’s lymphoma. N Engl J Med 2006; 354(23): 2431–2442
https://doi.org/10.1056/NEJMoa055759
pmid: 16760443
|
56 |
Recaldin T, Fear DJ. Transcription factors regulating B cell fate in the germinal centre. Clin Exp Immunol 2016; 183(1): 65–75
https://doi.org/10.1111/cei.12702
pmid: 26352785
|
57 |
Ramezani-Rad P, Rickert RC. Murine models of germinal center derived-lymphomas. Curr Opin Immunol 2017; 45: 31–36
https://doi.org/10.1016/j.coi.2016.12.002
pmid: 28160624
|
58 |
Basso K, Dalla-Favera R. Germinal centres and B cell lymphomagenesis. Nat Rev Immunol 2015; 15(3): 172–184
https://doi.org/10.1038/nri3814
pmid: 25712152
|
59 |
Dorsett Y, Robbiani DF, Jankovic M, Reina-San-Martin B, Eisenreich TR, Nussenzweig MC. A role for AID in chromosome translocations between c-myc and the IgH variable region. J Exp Med 2007; 204(9): 2225–2232
https://doi.org/10.1084/jem.20070884
pmid: 17724134
|
60 |
Pasqualucci LBhagat G, Jankovic M, Compagno M, Smith P, Muramatsu M, Honjo T, Morse HC, Nussenzweig MC 3rd, Dalla-Favera R. AID is required for germinal center-derived lymphomagenesis. Nat Genet 2008; 40(1): 108–112
https://doi.org/10.1038/ng.2007.35
pmid: 18066064
|
61 |
Victora GD, Dominguez-Sola D, Holmes AB, Deroubaix S, Dalla-Favera R, Nussenzweig MC. Identification of human germinal center light and dark zone cells and their relationship to human B-cell lymphomas. Blood 2012; 120(11): 2240–2248
https://doi.org/10.1182/blood-2012-03-415380
pmid: 22740445
|
62 |
Schmitz R, Ceribelli M, Pittaluga S, Wright G, Staudt LM. Oncogenic mechanisms in Burkitt lymphoma. Cold Spring Harb Perspect Med 2014; 4(2): a014282
https://doi.org/10.1101/cshperspect.a014282
pmid: 24492847
|
63 |
Gloury R, Zotos D, Zuidscherwoude M, Masson F, Liao Y, Hasbold J, Corcoran LM, Hodgkin PD, Belz GT, Shi W, Nutt SL, Tarlinton DM, Kallies A. Dynamic changes in Id3 and E-protein activity orchestrate germinal center and plasma cell development. J Exp Med 2016; 213(6): 1095–1111
https://doi.org/10.1084/jem.20152003
pmid: 27217539
|
64 |
Calado DP, Sasaki Y, Godinho SA, Pellerin A, Köchert K, Sleckman BP, de Alborán IM, Janz M, Rodig S, Rajewsky K. The cell-cycle regulator c-Myc is essential for the formation and maintenance of germinal centers. Nat Immunol 2012; 13(11): 1092–1100
https://doi.org/10.1038/ni.2418
pmid: 23001146
|
65 |
Dominguez-Sola D, Victora GD, Ying CY, Phan RT, Saito M, Nussenzweig MC, Dalla-Favera R. The proto-oncogene MYC is required for selection in the germinal center and cyclic reentry. Nat Immunol 2012; 13(11): 1083–1091
https://doi.org/10.1038/ni.2428
pmid: 23001145
|
66 |
Bemark M, Neuberger MS. By-products of immunoglobulin somatic hypermutation. Genes Chromosomes Cancer 2003; 38(1): 32–39
https://doi.org/10.1002/gcc.10241
pmid: 12874784
|
67 |
Guikema JE, de Boer C, Haralambieva E, Smit LA, van Noesel CJ, Schuuring E, Kluin PM. IGH switch breakpoints in Burkitt lymphoma: exclusive involvement of noncanonical class switch recombination. Genes Chromosomes Cancer 2006; 45(9): 808–819
https://doi.org/10.1002/gcc.20345
pmid: 16736499
|
68 |
Xu Z, Pone EJ, Al-Qahtani A, Park SR, Zan H, Casali P. Regulation of aicda expression and AID activity: relevance to somatic hypermutation and class switch DNA recombination. Crit Rev Immunol 2007; 27(4): 367–397
https://doi.org/10.1615/CritRevImmunol.v27.i4.60
pmid: 18197815
|
69 |
Basso K, Dalla-Favera R. Roles of BCL6 in normal and transformed germinal center B cells. Immunol Rev 2012; 247(1): 172–183
https://doi.org/10.1111/j.1600-065X.2012.01112.x
pmid: 22500840
|
70 |
Cruz-Rodriguez N, Combita AL, Enciso LJ, Raney LF, Pinzon PL, Lozano OC, Campos AM, Peñaloza N, Solano J, Herrera MV, Zabaleta J, Quijano S. Prognostic stratification improvement by integrating ID1/ID3/IGJ gene expression signature and immunophenotypic profile in adult patients with B-ALL. J Exp Clin Cancer Res 2017; 36(1): 37
https://doi.org/10.1186/s13046-017-0506-4
pmid: 28245840
|
71 |
Bellido M, Aventín A, Lasa A, Estivill C, Carnicer MJ, Pons C, Matías-Guiu X, Bordes R, Baiget M, Sierra J, Nomdedéu JF. Id4 is deregulated by a t(6;14)(p22;q32) chromosomal translocation in a B-cell lineage acute lymphoblastic leukemia. Haematologica 2003; 88(9): 994–1001
pmid: 12969807
|
72 |
Mandelbaum J, Bhagat G, Tang H, Mo T, Brahmachary M, Shen Q, Chadburn A, Rajewsky K, Tarakhovsky A, Pasqualucci L, Dalla-Favera R. BLIMP1 is a tumor suppressor gene frequently disrupted in activated B cell-like diffuse large B cell lymphoma. Cancer Cell 2010; 18(6): 568–579
https://doi.org/10.1016/j.ccr.2010.10.030
pmid: 21156281
|
73 |
Husson H, Carideo EG, Neuberg D, Schultze J, Munoz O, Marks PW, Donovan JW, Chillemi AC, O’Connell P, Freedman AS. Gene expression profiling of follicular lymphoma and normal germinal center B cells using cDNA arrays. Blood 2002; 99(1): 282–289
https://doi.org/10.1182/blood.V99.1.282
pmid: 11756183
|
74 |
Renné C, Martin-Subero JI, Eickernjäger M, Hansmann ML, Küppers R, Siebert R, Bräuninger A. Aberrant expression of ID2, a suppressor of B-cell-specific gene expression, in Hodgkin’s lymphoma. Am J Pathol 2006; 169(2): 655–664
https://doi.org/10.2353/ajpath.2006.060020
pmid: 16877363
|
75 |
Mathas S, Janz M, Hummel F, Hummel M, Wollert-Wulf B, Lusatis S, Anagnostopoulos I, Lietz A, Sigvardsson M, Jundt F, Jöhrens K, Bommert K, Stein H, Dörken B. Intrinsic inhibition of transcription factor E2A by HLH proteins ABF-1 and Id2 mediates reprogramming of neoplastic B cells in Hodgkin lymphoma. Nat Immunol 2006; 7(2): 207–215
https://doi.org/10.1038/ni1285
pmid: 16369535
|
76 |
Küppers R, Bräuninger A. Reprogramming of the tumour B-cell phenotype in Hodgkin lymphoma. Trends Immunol 2006; 27(5): 203–205
https://doi.org/10.1016/j.it.2006.03.001
pmid: 16563865
|
77 |
Zhao P, Lu Y, Liu L, Zhong M. Aberrant expression of ID2 protein and its correlation with EBV-LMP1 and P16(INK4A) in classical Hodgkin lymphoma in China. BMC Cancer 2008; 8(1): 379
https://doi.org/10.1186/1471-2407-8-379
pmid: 19099554
|
78 |
Ikeda JI, Wada N, Nojima S, Tahara S, Tsuruta Y, Oya K, Morii E. ID1 upregulation and FoxO3a downregulation by Epstein-Barr virus-encoded LMP1 in Hodgkin’s lymphoma. Mol Clin Oncol 2016; 5(5): 562–566
https://doi.org/10.3892/mco.2016.1012
pmid: 27900085
|
79 |
Lietz A, Janz M, Sigvardsson M, Jundt F, Dörken B, Mathas S. Loss of bHLH transcription factor E2A activity in primary effusion lymphoma confers resistance to apoptosis. Br J Haematol 2007; 137(4): 342–348
https://doi.org/10.1111/j.1365-2141.2007.06583.x
pmid: 17456056
|
80 |
Liu TY, Chen SU, Kuo SH, Cheng AL, Lin CW. E2A-positive gastric MALT lymphoma has weaker plasmacytoid infiltrates and stronger expression of the memory B-cell-associated miR-223: possible correlation with stage and treatment response. Mod Pathol 2010; 23(11): 1507–1517
https://doi.org/10.1038/modpathol.2010.139
pmid: 20802470
|
81 |
Seidel MG, Look AT. E2A-HLF usurps control of evolutionarily conserved survival pathways. Oncogene 2001; 20(40): 5718–5725
https://doi.org/10.1038/sj.onc.1204591
pmid: 11607821
|
82 |
Yoshihara T, Inaba T, Shapiro LH, Kato JY, Look AT. E2A-HLF-mediated cell transformation requires both the trans-activation domains of E2A and the leucine zipper dimerization domain of HLF. Mol Cell Biol 1995; 15(6): 3247–3255
https://doi.org/10.1128/MCB.15.6.3247
pmid: 7760820
|
83 |
Kamps MP, Baltimore D. E2A-Pbx1, the t(1;19) translocation protein of human pre-B-cell acute lymphocytic leukemia, causes acute myeloid leukemia in mice. Mol Cell Biol 1993; 13(1): 351–357
https://doi.org/10.1128/MCB.13.1.351
pmid: 8093327
|
84 |
Dedera DA, Waller EK, LeBrun DP, Sen-Majumdar A, Stevens ME, Barsh GS, Cleary ML. Chimeric homeobox gene E2A-PBX1 induces proliferation, apoptosis, and malignant lymphomas in transgenic mice. Cell 1993; 74(5): 833–843
https://doi.org/10.1016/0092-8674(93)90463-Z
pmid: 8104101
|
85 |
Nourse J, Mellentin JD, Galili N, Wilkinson J, Stanbridge E, Smith SD, Cleary ML. Chromosomal translocation t(1;19) results in synthesis of a homeobox fusion mRNA that codes for a potential chimeric transcription factor. Cell 1990; 60(4): 535–545
https://doi.org/10.1016/0092-8674(90)90657-Z
pmid: 1967982
|
86 |
Engel I, Murre C. The function of E- and Id proteins in lymphocyte development. Nat Rev Immunol 2001; 1(3): 193–199
https://doi.org/10.1038/35105060
pmid: 11905828
|
87 |
Murre C. Role of helix-loop-helix proteins in lymphocyte development. Cold Spring Harb Symp Quant Biol 1999; 64(0): 39–44
https://doi.org/10.1101/sqb.1999.64.39
pmid: 11232313
|
88 |
Miyazaki M, Rivera RR, Miyazaki K, Lin YC, Agata Y, Murre C. The opposing roles of the transcription factor E2A and its antagonist Id3 that orchestrate and enforce the naive fate of T cells. Nat Immunol 2011; 12(10): 992–1001
https://doi.org/10.1038/ni.2086
pmid: 21857655
|
89 |
Bain G, Engel I, Robanus Maandag EC, te Riele HP, Voland JR, Sharp LL, Chun J, Huey B, Pinkel D, Murre C. E2A deficiency leads to abnormalities in αβ T-cell development and to rapid development of T-cell lymphomas. Mol Cell Biol 1997; 17(8): 4782–4791
https://doi.org/10.1128/MCB.17.8.4782
pmid: 9234734
|
90 |
Yan W, Young AZ, Soares VC, Kelley R, Benezra R, Zhuang Y. High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol Cell Biol 1997; 17(12): 7317–7327
https://doi.org/10.1128/MCB.17.12.7317
pmid: 9372963
|
91 |
Engel I, Murre C. Ectopic expression of E47 or E12 promotes the death of E2A-deficient lymphomas. Proc Natl Acad Sci USA 1999; 96(3): 996–1001
https://doi.org/10.1073/pnas.96.3.996
pmid: 9927682
|
92 |
Sicinska E, Aifantis I, Le Cam L, Swat W, Borowski C, Yu Q, Ferrando AA, Levin SD, Geng Y, von Boehmer H, Sicinski P. Requirement for cyclin D3 in lymphocyte development and T cell leukemias. Cancer Cell 2003; 4(6): 451–461
https://doi.org/10.1016/S1535-6108(03)00301-5
pmid: 14706337
|
93 |
Schwartz R, Engel I, Fallahi-Sichani M, Petrie HT, Murre C. Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development. Proc Natl Acad Sci USA 2006; 103(26): 9976–9981
https://doi.org/10.1073/pnas.0603728103
pmid: 16782810
|
94 |
Steininger A, Möbs M, Ullmann R, Köchert K, Kreher S, Lamprecht B, Anagnostopoulos I, Hummel M, Richter J, Beyer M, Janz M, Klemke CD, Stein H, Dörken B, Sterry W, Schrock E, Mathas S, Assaf C. Genomic loss of the putative tumor suppressor gene E2A in human lymphoma. J Exp Med 2011; 208(8): 1585–1593
https://doi.org/10.1084/jem.20101785
pmid: 21788410
|
95 |
Mathas S, Kreher S, Meaburn KJ, Jöhrens K, Lamprecht B, Assaf C, Sterry W, Kadin ME, Daibata M, Joos S, Hummel M, Stein H, Janz M, Anagnostopoulos I, Schrock E, Misteli T, Dörken B. Gene deregulation and spatial genome reorganization near breakpoints prior to formation of translocations in anaplastic large cell lymphoma. Proc Natl Acad Sci USA 2009; 106(14): 5831–5836
https://doi.org/10.1073/pnas.0900912106
pmid: 19321746
|
96 |
O’Neil J, Shank J, Cusson N, Murre C, Kelliher M. TAL1/SCL induces leukemia by inhibiting the transcriptional activity of E47/HEB. Cancer Cell 2004; 5(6): 587–596
https://doi.org/10.1016/j.ccr.2004.05.023
pmid: 15193261
|
97 |
Park ST, Nolan GP, Sun XH. Growth inhibition and apoptosis due to restoration of E2A activity in T cell acute lymphoblastic leukemia cells. J Exp Med 1999; 189(3): 501–508
https://doi.org/10.1084/jem.189.3.501
pmid: 9927512
|
98 |
Sanda T, Lawton LN, Barrasa MI, Fan ZP, Kohlhammer H, Gutierrez A, Ma W, Tatarek J, Ahn Y, Kelliher MA, Jamieson CH, Staudt LM, Young RA, Look AT. Core transcriptional regulatory circuit controlled by the TAL1 complex in human T cell acute lymphoblastic leukemia. Cancer Cell 2012; 22(2): 209–221
https://doi.org/10.1016/j.ccr.2012.06.007
pmid: 22897851
|
99 |
Tan SH, Yam AW, Lawton LN, Wong RW, Young RA, Look AT, Sanda T. TRIB2 reinforces the oncogenic transcriptional program controlled by the TAL1 complex in T-cell acute lymphoblastic leukemia. Leukemia 2016; 30(4): 959–962
https://doi.org/10.1038/leu.2015.195
pmid: 26202930
|
100 |
Spaulding C, Reschly EJ, Zagort DE, Yashiro-Ohtani Y, Beverly LJ, Capobianco A, Pear WS, Kee BL. Notch1 co-opts lymphoid enhancer factor 1 for survival of murine T-cell lymphomas. Blood 2007; 110(7): 2650–2658
https://doi.org/10.1182/blood-2007-04-084202
pmid: 17585052
|
101 |
Wang HC, Peng V, Zhao Y, Sun XH. Enhanced Notch activation is advantageous but not essential for T cell lymphomagenesis in Id1 transgenic mice. PLoS One 2012; 7(2): e32944
https://doi.org/10.1371/journal.pone.0032944
pmid: 22393458
|
102 |
Grabher C, von Boehmer H, Look AT. Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nat Rev Cancer 2006; 6(5): 347–359
https://doi.org/10.1038/nrc1880
pmid: 16612405
|
103 |
Reschly EJ, Spaulding C, Vilimas T, Graham WV, Brumbaugh RL, Aifantis I, Pear WS, Kee BL. Notch1 promotes survival of E2A-deficient T cell lymphomas through pre-T cell receptor-dependent and-independent mechanisms. Blood 2006; 107(10): 4115–4121
https://doi.org/10.1182/blood-2005-09-3551
pmid: 16449526
|
104 |
Talora C, Campese AF, Bellavia D, Pascucci M, Checquolo S, Groppioni M, Frati L, von Boehmer H, Gulino A, Screpanti I. Pre-TCR-triggered ERK signalling-dependent downregulation of E2A activity in Notch3-induced T-cell lymphoma. EMBO Rep 2003; 4(11): 1067–1072
https://doi.org/10.1038/sj.embor.7400013
pmid: 14566327
|
105 |
Cotta CV, Leventaki V, Atsaves V, Vidaki A, Schlette E, Jones D, Medeiros LJ, Rassidakis GZ. The helix-loop-helix protein Id2 is expressed differentially and induced by myc in T-cell lymphomas. Cancer 2008; 112(3): 552–561
https://doi.org/10.1002/cncr.23196
pmid: 18085637
|
106 |
Morrow MA, Mayer EW, Perez CA, Adlam M, Siu G. Overexpression of the helix-loop-helix protein Id2 blocks T cell development at multiple stages. Mol Immunol 1999; 36(8): 491–503
https://doi.org/10.1016/S0161-5890(99)00071-1
pmid: 10475604
|
107 |
Kim D, Peng XC, Sun XH. Massive apoptosis of thymocytes in T-cell-deficient Id1 transgenic mice. Mol Cell Biol 1999; 19(12): 8240–8253
https://doi.org/10.1128/MCB.19.12.8240
pmid: 10567549
|
108 |
Li J, Maruyama T, Zhang P, Konkel JE, Hoffman V, Zamarron B, Chen W. Mutation of inhibitory helix-loop-helix protein Id3 causes gd T-cell lymphoma in mice. Blood 2010; 116(25): 5615–5621
https://doi.org/10.1182/blood-2010-03-274506
pmid: 20852128
|
109 |
Li J, Roy S, Kim YM, Li S, Zhang B, Love C, Reddy A, Rajagopalan D, Dave S, Diehl AM, Zhuang Y. Id2 collaborates with Id3 to suppress invariant NKT and innate-like tumors. J Immunol 2017; 198(8): 3136–3148
https://doi.org/10.4049/jimmunol.1601935
pmid: 28258199
|
110 |
Miyazaki M, Miyazaki K, Chen S, Chandra V, Wagatsuma K, Agata Y, Rodewald HR, Saito R, Chang AN, Varki N, Kawamoto H, Murre C. The E-Id protein axis modulates the activities of the PI3K-AKT-mTORC1-Hif1a and c-myc/p19Arf pathways to suppress innate variant TFH cell development, thymocyte expansion, and lymphomagenesis. Genes Dev 2015; 29(4): 409–425
https://doi.org/10.1101/gad.255331.114
pmid: 25691468
|
111 |
Yu L, Liu C, Vandeusen J, Becknell B, Dai Z, Wu YZ, Raval A, Liu TH, Ding W, Mao C, Liu S, Smith LT, Lee S, Rassenti L, Marcucci G, Byrd J, Caligiuri MA, Plass C. Global assessment of promoter methylation in a mouse model of cancer identifies ID4 as a putative tumor-suppressor gene in human leukemia. Nat Genet 2005; 37(3): 265–274
https://doi.org/10.1038/ng1521
pmid: 15723065
|
112 |
Chen SS, Claus R, Lucas DM, Yu L, Qian J, Ruppert AS, West DA, Williams KE, Johnson AJ, Sablitzky F, Plass C, Byrd JC. Silencing of the inhibitor of DNA binding protein 4 (ID4) contributes to the pathogenesis of mouse and human CLL. Blood 2011; 117(3): 862–871
https://doi.org/10.1182/blood-2010-05-284638
pmid: 21098398
|
113 |
Cen J, Shen J, Wang X, Kang H, Wang L, Sun L, Li Y, Yu L. Association between lymphoma prognosis and aberrant methylation of ID4 and ZO-1 in bone marrow and paraffin-embedded lymphoma tissues of treatment-naive patients. Oncol Rep 2013; 30(1): 455–461
https://doi.org/10.3892/or.2013.2450
pmid: 23670122
|
114 |
Hagiwara K, Nagai H, Li Y, Ohashi H, Hotta T, Saito H. Frequent DNA methylation but not mutation of the ID4 gene in malignant lymphoma. J Clin Exp Hematop 2007; 47(1): 15–18
https://doi.org/10.3960/jslrt.47.15
pmid: 17510533
|
115 |
Alani RM, Hasskarl J, Grace M, Hernandez MC, Israel MA, Münger K. Immortalization of primary human keratinocytes by the helix-loop-helix protein, Id-1. Proc Natl Acad Sci USA 1999; 96(17): 9637–9641
https://doi.org/10.1073/pnas.96.17.9637
pmid: 10449746
|
116 |
Nickoloff BJ, Chaturvedi V, Bacon P, Qin JZ, Denning MF, Diaz MO. Id-1 delays senescence but does not immortalize keratinocytes. J Biol Chem 2000; 275(36): 27501–27504
pmid: 10908559
|
117 |
Wöhner M, Tagoh H, Bilic I, Jaritz M, Poliakova DK, Fischer M, Busslinger M. Molecular functions of the transcription factors E2A and E2-2 in controlling germinal center B cell and plasma cell development. J Exp Med 2016; 213(7): 1201–1221
https://doi.org/10.1084/jem.20152002
pmid: 27261530
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