Genome-wide analyses identify KLF4 as an important negative regulator in T-cell acute lymphoblastic leukemia through directly inhibiting T-cell associated genes

Molecular Cancer

Volumn 14, Issue 1, 2015, Pages

  Li, Wei ^a   Jiang, Zhiwu ^a   Li, Tianzhong ^a   Wei, Xinru ^a   Zheng, Yi ^a   Wu, Donghai ^a   Yang, Lijian ^b,c   Chen, Shaohua ^b,c   Xu, Bing ^d   Zhong, Mei ^e   Jiang, Jue ^f   Hu, Yufeng ^f   Su, Hexiu ^f   Zhang, Minjie ^g   Huang, Xiaojun ^h   Geng, Suxia ⁱ   Weng, Jianyu ⁱ   Du, Xin ⁱ   Liu, Pentao ^j   Li, Yangqiu ^b,c   Liu, Hudan ^f   Yao, Yao ^a   Li, Peng ^a   more..

^a GUANGZHOU INSTITUTES OF BIOMEDICINE AND HEALTH   (China)

^b MEDICAL COLLEGE OF JINAN UNIVERSITY   (China)

^c JINAN UNIVERSITY   (China)

^d SOUTHERN MEDICAL UNIVERSITY   (China)

^e FIRST MILITARY MEDICAL UNIVERSITY   (China)

^f HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^g University Town of Shenzhen   (China)

^h PEKING UNIVERSITY PEOPLE S HOSPITAL   (China)

ⁱ GUANGDONG PROVINCIAL PEOPLE'S HOSPITAL   (China)

^j WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

more..

Author keywords

Apoptosis; BCL11B; KLF4; NOTCH1; T cell; T ALL

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; KRUPPEL LIKE FACTOR 4; NOTCH1 RECEPTOR; PEPTIDES AND PROTEINS; PROTEIN BCL 11B; PROTEIN BCL 2; PROTEIN BCL XL; RNA; TRANSCRIPTION FACTOR 7; TRANSCRIPTION FACTOR GATA 3; UNCLASSIFIED DRUG; BCL11B PROTEIN, HUMAN; BCL2L1 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; PROTEIN BCL X; REPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BINDING SITE; CANCER SURVIVAL; CONTROLLED STUDY; GENOME ANALYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; JURKAT CELL LINE; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SEQUENCE; SIGNAL TRANSDUCTION; SUMOYLATION; T CELL LYMPHOBLASTIC LEUKEMIA CELL; T LYMPHOCYTE; TUMOR INVASION; TUMOR XENOGRAFT; ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL; BIOLOGICAL MODEL; CLUSTER ANALYSIS; DISEASE COURSE; DISEASE MODEL; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETICS; METABOLISM; XENOGRAFT;

ANIMALS; APOPTOSIS; BCL-X PROTEIN; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOWN-REGULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, LEUKEMIC; GENOME-WIDE ASSOCIATION STUDY; HETEROGRAFTS; HUMANS; JURKAT CELLS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MODELS, BIOLOGICAL; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-BCL-2; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SUMOYLATION; TUMOR SUPPRESSOR PROTEINS;

EID: 84961512480     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/s12943-014-0285-x     Document Type: Article

References (55)

1. Ghaleb AM, Nandan MO, Chanchevalap S, Dalton WB, Hisamuddin IM, Yang VW. Kruppel-like factors 4 and 5: the yin and yang regulators of cellular proliferation. Cell Res. 2005;15(2):92-6.
2. Wei D, Kanai M, Huang S, Xie K. Emerging role of KLF4 in human gastrointestinal cancer. Carcinogenesis. 2006;27(1):23-31.
3. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126 (4):663-76.
4. Kim J, Chu J, Shen X, Wang J, Orkin SH. An extended transcriptional network for pluripotency of embryonic stem cells. Cell. 2008;132(6):1049-61.
5. Segre JA, Bauer C, Fuchs E. Klf4 is a transcription factor required for establishing the barrier function of the skin. Nat Genet. 1999;22(4):356-60.
6. Wen X, Liu H, Xiao G, Liu X. Downregulation of the transcription factor KLF4 is required for the lineage commitment of T cells. Cell Res. 2011;21(12):1701-10.
7. Ciofani M, Zuniga-Pflucker JC. The thymus as an inductive site for T lymphopoiesis. Annu Rev Cell Dev Biol. 2007;23:463-93.
8. Weber BN, Chi AW, Chavez A, Yashiro-Ohtani Y, Yang Q, Shestova O, et al. A critical role for TCF-1 in T-lineage specification and differentiation. Nature. 2011;476(7358):63-8.
9. Liu P, Li P, Burke S. Critical roles of Bcl11b in T-cell development and maintenance of T-cell identity. Immunol Rev. 2010;238(1):138-49.
10. Hosoya T, Maillard I, Engel JD. From the cradle to the grave: activities of GATA-3 throughout T-cell development and differentiation. Immunol Rev. 2010;238(1):110-25.
11. Radtke F, Wilson A, MacDonald HR. Notch signaling in T- and B-cell development. Curr Opin Immunol. 2004;16(2):174-9.
12. Radtke F, Wilson A, Stark G, Bauer M, van Meerwijk J, MacDonald HR, et al. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity. 1999;10(5):547-58.
13. Li P, Burke S, Wang J, Chen X, Ortiz M, Lee SC, et al. Reprogramming of T cells to natural killer-like cells upon Bcl11b deletion. Science. 2010;329(5987):85-9.
14. Van Nguyen T, Angkasekwinai P, Dou H, Lin FM, Lu LS, Cheng J, et al. SUMO-specific protease 1 is critical for early lymphoid development through regulation of STAT5 activation. Mol Cell. 2012;45(2):210-21.
15. Zhang LJ, Vogel WK, Liu X, Topark-Ngarm A, Arbogast BL, Maier CS, et al. Coordinated regulation of transcription factor Bcl11b activity in thymocytes by the mitogen-activated protein kinase (MAPK) pathways and protein sumoylation. J Biol Chem. 2012;287(32):26971-88.
16. Aifantis I, Raetz E, Buonamici S. Molecular pathogenesis of T-cell leukaemia and lymphoma. Nat Rev Immunol. 2008;8(5):380-90.
17. Weng AP, Ferrando AA, Lee W, Morris JPT, Silverman LB, Sanchez-Irizarry C, et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science. 2004;306(5694):269-71.
18. Lin YW, Nichols RA, Letterio JJ, Aplan PD. Notch1 mutations are important for leukemic transformation in murine models of precursor-T leukemia/ lymphoma. Blood. 2006;107(6):2540-3.
19. Przybylski GK, Dik WA, Wanzeck J, Grabarczyk P, Majunke S, Martin-Subero JI, et al. Disruption of the BCL11B gene through inv(14)(q11.2q32.31) results in the expression of BCL11B-TRDC fusion transcripts and is associated with the absence of wild-type BCL11B transcripts in T-ALL. Leukemia. 2005;19(2):201-8.
20. Gutierrez A, Kentsis A, Sanda T, Holmfeldt L, Chen SC, Zhang J, et al. The BCL11B tumor suppressor is mutated across the major molecular subtypes of T-cell acute lymphoblastic leukemia. Blood. 2011;118(15):4169-73.
21. Yasunaga J, Taniguchi Y, Nosaka K, Yoshida M, Satou Y, Sakai T, et al. Identification of aberrantly methylated genes in association with adult T-cell leukemia. Cancer Res. 2004;64(17):6002-9.
22. Malik D, Kaul D, Chauhan N, Marwaha RK. miR-2909-mediated regulation of KLF4: a novel molecular mechanism for differentiating between B-cell and T-cell pediatric acute lymphoblastic leukemias. Mol Cancer. 2014;13:175.
23. Beckwith M, Longo DL, O'Connell CD, Moratz CM, Urba WJ. Phorbol ester-induced, cell-cycle-specific, growth inhibition of human B-lymphoma cell lines. J Natl Cancer Inst. 1990;82(6):501-9.
24. Ortaldo JR, Oldham RK, Cannon GC, Herberman RB. Specificity of natural cytotoxic reactivity of normal human lymphocytes against a myeloid leukemia cell line. J Natl Cancer Inst. 1977;59(1):77-82.
25. Abadir AM, Lang A, Klein T, Abenhaim HA. Influence of qualitative research on women's health screening guidelines. Am J Obstet Gynecol. 2014;210(1):44. e1-6.
26. Tsuno T, Mejido J, Zhao T, Phillips T, Myers TG, Bekisz J, et al. BID is a critical factor controlling cell viability regulated by IFN-alpha. J Immunother. 2012;35(1):23-31.
27. Bao L, Odell AF, Stephen SL, Wheatcroft SB, Walker JH, Ponnambalam S. The S100A6 calcium-binding protein regulates endothelial cell-cycle progression and senescence. FEBS J. 2012;279(24):4576-88.
28. de Bock CE, Ardjmand A, Molloy TJ, Bone SM, Johnstone D, Campbell DM, et al. The Fat1 cadherin is overexpressed and an independent prognostic factor for survival in paired diagnosis-relapse samples of precursor B-cell acute lymphoblastic leukemia. Leukemia. 2012;26 (5):918-26.
29. Deng X, Ma Q, Zhang B, Jiang H, Zhang Z, Wang Y. Migration-stimulating factor (MSF) is over-expressed in non-small cell lung cancer and promotes cell migration and invasion in A549 cells over-expressing MSF. Exp Cell Res. 2013;319(17):2545-53.
30. Ferone G, Mollo MR, Thomason HA, Antonini D, Zhou H, Ambrosio R, et al. p63 control of desmosome gene expression and adhesion is compromised in AEC syndrome. Hum Mol Genet. 2013;22(3):531-43.
31. Chinnadurai G, Vijayalingam S, Rashmi R. BIK, the founding member of the BH3-only family proteins: mechanisms of cell death and role in cancer and pathogenic processes. Oncogene. 2008;27 Suppl 1:S20-9.
32. Buonamici S, Trimarchi T, Ruocco MG, Reavie L, Cathelin S, Mar BG, et al. CCR7 signalling as an essential regulator of CNS infiltration in T-cell leukaemia. Nature. 2009;459(7249):1000-4.
33. Hoggatt J, Pelus LM. Eicosanoid regulation of hematopoiesis and hematopoietic stem and progenitor trafficking. Leukemia. 2010;24(12):1993-2002.
34. Kawaguchi A, Orba Y, Kimura T, Iha H, Ogata M, Tsuji T, et al. Inhibition of the SDF-1alpha-CXCR4 axis by the CXCR4 antagonist AMD3100 suppresses the migration of cultured cells from ATL patients and murine lymphoblastoid cells from HTLV-I Tax transgenic mice. Blood. 2009;114(14):2961-8.
35. Saraiva N, Prole DL, Carrara G, Johnson BF, Taylor CW, Parsons M, et al. hGAAP promotes cell adhesion and migration via the stimulation of storeoperated Ca2+ entry and calpain 2. J Cell Biol. 2013;202(4):699-713.
36. Sabatier L, Djokic J, Fagotto-Kaufmann C, Chen M, Annis DS, Mosher DF, et al. Complex contributions of fibronectin to initiation and maturation of microfibrils. Biochem J. 2013;456(2):283-95.
37. Abaeva AA, Canault M, Kotova YN, Obydennyy SI, Yakimenko AO, Podoplelova NA, et al. Procoagulant platelets form an alpha-granule protein-covered "cap" on their surface that promotes their attachment to aggregates. J Biol Chem. 2013;288(41):29621-32.
38. Patel B, Kang Y, Cui K, Litt M, Riberio MS, Deng C, et al. Aberrant TAL1 activation is mediated by an interchromosomal interaction in human T-cell acute lymphoblastic leukemia. Leukemia. 2014;28(2):349-61.
39. Liu P, Keller JR, Ortiz M, Tessarollo L, Rachel RA, Nakamura T, et al. Bcl11a is essential for normal lymphoid development. Nat Immunol. 2003;4(6):525-32.
40. Cain DW, O'Koren EG, Kan MJ, Womble M, Sempowski GD, Hopper K, et al. Identification of a tissue-specific, C/EBPbeta-dependent pathway of differentiation for murine peritoneal macrophages. J Immunol. 2013;191(9):4665-75.
41. Johnson KD, Hsu AP, Ryu MJ, Wang J, Gao X, Boyer ME, et al. Cis-element mutated in GATA2-dependent immunodeficiency governs hematopoiesis and vascular integrity. J Clin Invest. 2012;122(10):3692-704.
42. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell. 2008;133(6):1106-17.
43. Tiwari N, Meyer-Schaller N, Arnold P, Antoniadis H, Pachkov M, van Nimwegen E, et al. Klf4 is a transcriptional regulator of genes critical for EMT, including Jnk1 (Mapk8). PLoS One. 2013;8(2):e57329.
44. Han Y, Amin HM, Frantz C, Franko B, Lee J, Lin Q, et al. Restoration of shp1 expression by 5-AZA-2'-deoxycytidine is associated with downregulation of JAK3/STAT3 signaling in ALK-positive anaplastic large cell lymphoma. Leukemia. 2006;20(9):1602-9.
45. Nishikawa Y, Miyazaki T, Nakashiro K, Yamagata H, Isokane M, Goda H, et al. Human FAT1 cadherin controls cell migration and invasion of oral squamous cell carcinoma through the localization of beta-catenin. Oncol Rep. 2011;26(3):587-92.
46. Real PJ, Ferrando AA. NOTCH inhibition and glucocorticoid therapy in T-cell acute lymphoblastic leukemia. Leukemia. 2009;23(8):1374-7.
47. Hale AT, Tian H, Anih E, Recio 3rd FO, Shatat MA, Johnson T, et al. Endothelial Kruppel-like factor 4 regulates angiogenesis and the Notch signaling pathway. J Biol Chem. 2014;289(17):12016-28.
48. Nagel S, Kaufmann M, Drexler HG, MacLeod RA. The cardiac homeobox gene NKX2-5 is deregulated by juxtaposition with BCL11B in pediatric T-ALL cell lines via a novel t(5;14)(q35.1;q32.2). Cancer Res. 2003;63(17):5329-34.
49. Grabarczyk P, Przybylski GK, Depke M, Volker U, Bahr J, Assmus K, et al. Inhibition of BCL11B expression leads to apoptosis of malignant but not normal mature T cells. Oncogene. 2007;26(26):3797-810.
50. Huang X, Chen S, Shen Q, Chen S, Yang L, Grabarczyk P, et al. Down regulation of BCL11B expression inhibits proliferation and induces apoptosis in malignant T cells by BCL11B-935-siRNA. Hematology. 2011;16(4):236-42.
51. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105-11.
52. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511-5.
53. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5(7):621-8.
54. Wang L, Feng Z, Wang X, Wang X, Zhang X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics. 2010;26(1):136-8.
55. Qing G, Li B, Vu A, Skuli N, Walton ZE, Liu X, et al. ATF4 regulates MYC-mediated neuroblastoma cell death upon glutamine deprivation. Cancer Cell. 2012;22(5):631-44.