Deregulation of Aiolos expression in chronic lymphocytic leukemia is associated with epigenetic modifications

Blood

Volumn 117, Issue 6, 2011, Pages 1917-1927

  Billot, Katy ^a   Soeur, Jérémie ^b   Chereau, Fanny ^c,d   Arrouss, Issam ^a   Merle Béral, Hélène ^a,d   Huang, Meng Er ^b   Mazier, Dominique ^a   Baud, Véronique ^c,d   Rebollo, Angelita ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b CNRS UMR3348   (France)

^c INSTITUT COCHIN   (France)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; IKAROS TRANSCRIPTION FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYSINE; TRANSCRIPTION FACTOR AIOLOS; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL MATURATION; CHRONIC LYMPHATIC LEUKEMIA; EPIGENETICS; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; MALE; PRIORITY JOURNAL;

EID: 79951497639     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-09-307140     Document Type: Article

References (50)

1. Matthias P, Rolink AG. Transcriptional networks in developing and mature B cells. Nat Rev Immunol. 2005;5(6):497-508. (Pubitemid 40835037)
2. Georgopoulos K, Moore DD, Derfler B. Ikaros, an early lymphoid-specific transcription factor and a putative mediator for T cell commitment. Science. 1992;258(5083):808-812.
3. Morgan B, Sun L, Avitahl N, et al. Aiolos, a lymphoid restricted transcription factor that interacts with Ikaros to regulate lymphocyte differentiation. EMBO J. 1997;16(8):2004-2013. (Pubitemid 27170961)
4. Caballero R, Setien F, Lopez-Serra L, et al. Combinatorial effects of splice variants modulate function of Aiolos. J Cell Sci. 2007;120(Pt 15):2619-2630. (Pubitemid 47323870)
5. Molnár A, Georgopoulos K. The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Mol Cell Biol. 1994;14(12):8292-8303.
6. Klug CA, Morrison SJ, Masek M, Hahm K, Smale ST, Weissman IL. Hematopoietic stem cells and lymphoid progenitors express different Ikaros isoforms, and Ikaros is localized to heterochromatin in immature lymphocytes. Proc Natl Acad Sci U S A. 1998;95(2):657-662. (Pubitemid 28083799)
7. Wang JH, Avitahl N, Cariappa A, et al. Aiolos regulates B cell activation and maturation to effector state. Immunity. 1998;9(4):543-553. (Pubitemid 28499205)
8. Billot K, Parizot C, Arrouss I, et al. Differential Aiolos expression in human hematopoietic subpopulations. Leuk Res. 2010;34(3):289-293.
9. Duhamel M, Arrouss I, Merle-Beral H, Rebollo A. The Aiolos transcription factor is up-regulated in chronic lymphocytic leukemia. Blood. 2008;111(6):3225-3228.
10. Nückel H, Frey UH, Sellmann L, Collins CH, Duhrsen U, Siffert W. The IKZF3 (Aiolos) transcription factor is highly up-regulated and inversely correlated with clinical progression in chronic lymphocytic leukaemia. Br J Haematol. 2009;144(2):268-270.
11. Matulic M, Paradzik M, Cicin-Sain L, et al. Ikaros family transcription factors in chronic and acute leukemia. Am J Hematol. 2009;84(6):375-377.
12. Chiorazzi N, Rai KR, Ferrarini M. Chronic lymphocytic leukemia. N Engl J Med. 2005;352(8):804-815.
13. Hamblin TJ, Davis Z, Gardiner A, Oscier DG, Stevenson FK. Unmutated Ig V(H) genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood. 1999;94(6):1848-1854. (Pubitemid 29430400)
14. Rosenwald A, Alizadeh AA, Widhopf G, et al. Relation of gene expression phenotype to immunoglobulin mutation genotype in B cell chronic lymphocytic leukemia. J Exp Med. 2001;194(11):1639-1647. (Pubitemid 33126814)
15. Mayr C, Speicher MR, Kofler DM, et al. Chromosomal translocations are associated with poor prognosis in chronic lymphocytic leukemia. Blood. 2006;107(2):742-751. (Pubitemid 43076401)
16. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007;128(4):683-692. (Pubitemid 46273572)
17. Mellor J. The dynamics of chromatin remodeling at promoters. Mol Cell. 2005;19(2):147-157. (Pubitemid 41019663)
18. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128(4):693-705. (Pubitemid 46273577)
19. Billot K, Arrouss I, Garcia-Alvarez G, et al. Deregulated Aiolos expression in common variable immunodeficiency. Open Immunol J. 2009;2:60-66.
20. Navarro P, Page DR, Avner P, Rougeulle C. Tsix-mediated epigenetic switch of a CTCF-flanked region of the Xist promoter determines the Xist transcription program. Genes Dev. 2006;20(20):2787-2792. (Pubitemid 44771741)
21. Jacque E, Tchenio T, Piton G, Romeo PH, Baud V. RelA repression of RelB activity induces selective gene activation downstream of TNF receptors. Proc Natl Acad Sci U S A. 2005;102(41):14635-14640. (Pubitemid 41457108)
22. Duhamel M, Navarro P, Cario-Andre M, Billot K, Arrouss I, Rebollo A. Differential epigenetic regulation of Aiolos expression in human tumoral cell lines and primary cells. FEBS Lett. 2008;582(3):457-467.
23. Romano MF, Lamberti A, Tassone P, et al. Triggering of CD40 antigen inhibits fludarabineinduced apoptosis in B chronic lymphocytic leukemia cells. Blood. 1998;92(3):990-995. (Pubitemid 28355483)
24. Ghadiri A, Duhamel M, Fleischer A, Reimann A, Dessauge F, Rebollo A. Critical function of Ikaros in controlling Aiolos gene expression. FEBS Lett. 2007;581(8):1605-1616. (Pubitemid 46528925)
25. Romero F, Martinez AC, Camonis J, Rebollo A. Aiolos transcription factor controls cell death in T cells by regulating Bcl-2 expression and its cellular localization. EMBO J. 1999;18(12):3419-3430. (Pubitemid 29276587)
26. Caligaris-Cappio F, Hamblin TJ. B-cell chronic lymphocytic leukemia: a bird of a different feather. J Clin Oncol. 1999;17(1):399-408. (Pubitemid 29022419)
27. Iacobucci I, Storlazzi CT, Cilloni D, et al. Identification and molecular characterization of recurrent genomic deletions on 7p12 in the IKZF1 gene in a large cohort of BCR-ABL1-positive acute lymphoblastic leukemia patients: on behalf of Gruppo Italiano Malattie Ematologiche dell'Adulto Acute Leukemia Working Party (GIMEMAAL WP). Blood. 2009;114(10):2159-2167.
28. Yagi T, Hibi S, Takanashi M, et al. High frequency of Ikaros isoform 6 expression in acute myelomonocytic and monocytic leukemias: implications for up-regulation of the antiapoptotic protein Bcl-XL in leukemogenesis. Blood. 2002;99(4):1350-1355. (Pubitemid 34547091)
29. Iacobucci I, Lonetti A, Cilloni D, et al. Identification of different Ikaros cDNA transcripts in Philadelphia-positive adult acute lymphoblastic leukemia by a high-throughput capillary electrophoresis sizing method. Haematologica. 2008;93(12):1814-1821.
30. Hamamoto R, Furukawa Y, Morita M, et al. SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells. Nat Cell Biol. 2004;6(8):731-740. (Pubitemid 39144478)
31. Hamamoto R, Silva FP, Tsuge M, et al. Enhanced SMYD3 expression is essential for the growth of breast cancer cells. Cancer Sci. 2006;97(2):113-118. (Pubitemid 43379478)
32. Silva FP, Hamamoto R, Kunizaki M, Tsuge M, Nakamura Y, Furukawa Y. Enhanced methyltransferase activity of SMYD3 by the cleavage of its N-terminal region in human cancer cells. Oncogene. 2008;27(19):2686-2692. (Pubitemid 351581465)
33. Kim J, Sif S, Jones B, et al. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity. 1999;10(3):345-355. (Pubitemid 29165289)
34. Rush LJ, Raval A, Funchain P, et al. Epigenetic profiling in chronic lymphocytic leukemia reveals novel methylation targets. Cancer Res. 2004;64(7):2424-2433. (Pubitemid 38523896)
35. Hanada M, Delia D, Aiello A, Stadtmauer E, Reed JC. bcl-2 gene hypomethylation and high-level expression in B-cell chronic lymphocytic leukemia. Blood. 1993;82(6):1820-1828. (Pubitemid 23278773)
36. Yuille MR, Condie A, Stone EM, et al. TCL1 is activated by chromosomal rearrangement or by hypomethylation. Genes Chromosomes Cancer. 2001;30(4):336-341. (Pubitemid 32216324)
37. Corcoran M, Parker A, Orchard J, et al. ZAP-70 methylation status is associated with ZAP-70 expression status in chronic lymphocytic leukemia. Haematologica. 2005;90(8):1078-1088. (Pubitemid 41323507)
38. Raval A, Tanner SM, Byrd JC, et al. Downregulation of death-associated protein kinase 1 (DAPK1) in chronic lymphocytic leukemia. Cell. 2007;129(5):879-890. (Pubitemid 46813150)
39. Pickering BM, de Mel S, Lee M, et al. Pharmacological inhibitors of NF-kappaB accelerate apoptosis in chronic lymphocytic leukaemia cells. Oncogene. 2007;26(8):1166-1177.
40. Furman RR, Asgary Z, Mascarenhas JO, Liou HC, Schattner EJ. Modulation of NF-kappa B activity and apoptosis in chronic lymphocytic leukemia B cells. J Immunol. 2000;164(4):2200-2206. (Pubitemid 30108780)
41. Bernal A, Pastore RD, Asgary Z, et al. Survival of leukemic B cells promoted by engagement of the antigen receptor. Blood. 2001;98(10):3050-3057.
42. Hewamana S, Lin TT, Rowntree C, et al. Rel is an independent biomarker of clinical outcome in chronic lymphocytic leukemia. J Clin Oncol. 2009;27(5):763-769.
43. Narvi E, Nera KP, Terho P, Mustonen L, Granberg J, Lassila O. Aiolos controls gene conversion and cell death in DT40 B cells. Scand J Immunol. 2007;65(6):503-513. (Pubitemid 46808848)
44. Kikuchi H, Yamashita K, Nakayama M, et al. Lacking of Aiolos accelerates pre-mature B cell apoptosis mediated by BCR signaling through elevation in cytochrome c release. Biochim Biophys Acta. 2009;1793(7):1304-1314.
45. Wang JH, Nichogiannopoulou A, Wu L, et al. Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity. 1996;5(6):537-549. (Pubitemid 27062064)
46. Lopez-Guerra M, Colomer D. NF-kappaB as a therapeutic target in chronic lymphocytic leukemia. Expert Opin Ther Targets. 2010;14(3):275-288.
47. Gupta SC, Sundaram C, Reuter S, Aggarwal BB. Inhibiting NF-kappaB activation by small molecules as a therapeutic strategy. Biochim Biophys Acta. 2010;1799(10-12):775-787.
48. Karray S, Merle-Beral H, Vazquez A, Gerard JP, Debre P, Galanaud P. Functional heterogeneity of B-CLL lymphocytes: dissociated responsiveness to growth factors and distinct requirements for a first activation signal. Blood. 1987;70(4):1105-1110. (Pubitemid 18022390)
49. Lanham S, Hamblin T, Oscier D, Ibbotson R, Stevenson F, Packham G. Differential signaling via surface IgM is associated with VH gene mutational status and CD38 expression in chronic lymphocytic leukemia. Blood. 2003;101(3):1087-1093. (Pubitemid 36139383)
50. Thompson EC, Cobb BS, Sabbattini P, et al. Ikaros DNA-binding proteins as integral components of B cell developmental-stage-specific regulatory circuits. Immunity. 2007;26(3):335-344. (Pubitemid 46413909)