Fli-1 Overexpression in Hematopoietic Progenitors Deregulates T Cell Development and Induces Pre-T Cell Lymphoblastic Leukaemia/Lymphoma

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Smeets, Monique F M A ^a   Chan, Angela C ^a   Dagger, Samantha ^b   Bradley, Cara K ^c   Wei, Andrew ^d   Izon, David J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c Gennea   (Australia)

^d MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NOTCH1 RECEPTOR; PROTEIN BCL 2; TRANSCRIPTION FACTOR FLI 1;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; DISEASE ASSOCIATION; FRIEND LEUKEMIA VIRUS INTEGRATION 1 GENE; GENE FUNCTION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMOGENESIS; MOUSE; NONHUMAN; NOTCH 1 GENE; PROTO ONCOGENE; UPREGULATION;

ANIMALS; CARCINOGENESIS; GENE EXPRESSION; HEMATOPOIETIC STEM CELLS; HUMANS; INTRACELLULAR SPACE; MICE; MICE, INBRED C57BL; ORGAN SPECIFICITY; PRECURSOR B-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTO-ONCOGENE PROTEIN C-FLI-1; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTOR, NOTCH1; RNA, MESSENGER; T-LYMPHOCYTES; UP-REGULATION;

EID: 84877137854     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062346     Document Type: Article

References (56)

1. Ben-David Y, Giddens EB, Letwin K, Bernstein A, (1991) Erythroleukemia induction by Friend murine leukemia virus: insertional activation of a new member of the ets gene family, Fli-1, closely linked to c-ets-1. Genes Dev 5: 908-918.
2. Delattre O, Zucman J, Melot T, Garau XS, Zucker JM, et al. (1994) The Ewing family of tumors-a subgroup of small-round-cell tumors defined by specific chimeric transcripts. N Engl J Med 331: 294-299.
3. Kawada H, Ito T, Pharr PN, Spyropoulos DD, Watson DK, et al. (2001) Defective megakaryopoiesis and abnormal erythroid development in Fli-1 gene-targeted mice. Int J Hematol 73: 463-468.
4. Starck J, Weiss-Gayet M, Gonnet C, Guyot B, Vicat JM, et al. (2010) Inducible Fli-1 gene deletion in adult mice modifies several myeloid lineage commitment decisions and accelerates proliferation arrest and terminal erythrocytic differentiation. Blood 116: 4795-4805.
5. Masuya M, Moussa O, Abe T, Deguchi T, Higuchi T, et al. (2005) Dysregulation of granulocyte, erythrocyte, and NK cell lineages in Fli-1 gene-targeted mice. Blood 105: 95-102.
6. Anderson MK, Hernandez-Hoyos G, Diamond RA, Rothenberg EV, (1999) Precise developmental regulation of Ets family transcription factors during specification and commitment to the T cell lineage. Development 126: 3131-3148.
7. Zhang L, Eddy A, Teng YT, Fritzler M, Kluppel M, et al. (1995) An immunological renal disease in transgenic mice that overexpress Fli-1, a member of the ets family of transcription factor genes. Mol Cell Biol 15: 6961-6970.
8. Anderson G, Harman BC, Hare KJ, Jenkinson EJ, (2000) Microenvironmental regulation of T cell development in the thymus. Semin Immunol 12: 457-464.
9. Carlyle JR, Michie AM, Furlonger C, Nakano T, Lenardo MJ, et al. (1997) Identification of a novel developmental stage marking lineage commitment of progenitor thymocytes. J Exp Med 186: 173-182.
10. Wu L, Li CL, Shortman K, (1996) Thymic dendritic cell precursors: relationship to the T lymphocyte lineage and phenotype of the dendritic cell progeny. J Exp Med 184: 903-911.
11. Balciunaite G, Ceredig R, Rolink AG, (2005) The earliest subpopulation of mouse thymocytes contains potent T, significant macrophage, and natural killer cell but no B-lymphocyte potential. Blood 105: 1930-1936.
12. Bell JJ, Bhandoola A, (2008) The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 452: 764-767.
13. Wada H, Masuda K, Satoh R, Kakugawa K, Ikawa T, et al. (2008) Adult T-cell progenitors retain myeloid potential. Nature 452: 768-772.
14. Godfrey DI, Kennedy J, Mombaerts P, Tonegawa S, Zlotnik A, (1994) Onset of TCR-beta gene rearrangement and role of TCR-beta expression during CD3-CD4-CD8- thymocyte differentiation. J Immunol 152: 4783-4792.
15. Kruisbeek AM, Haks MC, Carleton M, Michie AM, Zuniga-Pflucker JC, et al. (2000) Branching out to gain control: how the pre-TCR is linked to multiple functions. Immunol Today 21: 637-644.
16. Wilson A, Petrie HT, Scollay R, Shortman K, (1989) The acquisition of CD4 and CD8 during the differentiation of early thymocytes in short-term culture. Int Immunol 1: 605-612.
17. Kawamoto H, Ohmura K, Fujimoto S, Lu M, Ikawa T, et al. (2003) Extensive proliferation of T cell lineage-restricted progenitors in the thymus: an essential process for clonal expression of diverse T cell receptor beta chains. Eur J Immunol 33: 606-615.
18. Izon DJ, Punt JA, Xu L, Karnell FG, Allman D, et al. (2001) Notch1 regulates maturation of CD4+ and CD8+ thymocytes by modulating TCR signal strength. Immunity 14: 253-264.
19. Schmitt TM, Zuniga-Pflucker JC, (2002) Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17: 749-756.
20. Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, et al. (1991) Simplified mammalian DNA isolation procedure. Nucleic Acids Res 19: 4293.
21. Gartner F, Alt FW, Monroe R, Chu M, Sleckman BP, et al. (1999) Immature thymocytes employ distinct signaling pathways for allelic exclusion versus differentiation and expansion. Immunity 10: 537-546.
22. Lin YW, Nichols RA, Letterio JJ, Aplan PD, (2006) Notch1 mutations are important for leukemic transformation in murine models of precursor-T leukemia/lymphoma. Blood 107: 2540-2543.
23. Ashworth TD, Pear WS, Chiang MY, Blacklow SC, Mastio J, et al. (2010) Deletion-based mechanisms of Notch1 activation in T-ALL: key roles for RAG recombinase and a conserved internal translational start site in Notch1. Blood 116: 5455-5464.
24. Jeannet R, Mastio J, Macias-Garcia A, Oravecz A, Ashworth T, et al. (2010) Oncogenic activation of the Notch1 gene by deletion of its promoter in Ikaros-deficient T-ALL. Blood 116: 5443-5454.
25. Craig FE, Foon KA, (2008) Flow cytometric immunophenotyping for hematologic neoplasms. Blood 111: 3941-3967.
26. Pereira R, Quang CT, Lesault I, Dolznig H, Beug H, et al. (1999) FLI-1 inhibits differentiation and induces proliferation of primary erythroblasts. Oncogene 18: 1597-1608.
27. Weng AP, Ferrando AA, Lee W, Morris JPt, Silverman LB, et al. (2004) Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306: 269-271.
28. O'Neil J, Calvo J, McKenna K, Krishnamoorthy V, Aster JC, et al. (2006) Activating Notch1 mutations in mouse models of T-ALL. Blood 107: 781-785.
29. Zhang XK, Moussa O, LaRue A, Bradshaw S, Molano I, et al. (2008) The transcription factor Fli-1 modulates marginal zone and follicular B cell development in mice. J Immunol 181: 1644-1654.
30. Swat W, Shinkai Y, Cheng HL, Davidson L, Alt FW, (1996) Activated Ras signals differentiation and expansion of CD4+8+ thymocytes. Proc Natl Acad Sci U S A 93: 4683-4687.
31. Hawley RG, Fong AZ, Ngan BY, Hawley TS, (1995) Hematopoietic transforming potential of activated ras in chimeric mice. Oncogene 11: 1113-1123.
32. Winandy S, Wu P, Georgopoulos K, (1995) A dominant mutation in the Ikaros gene leads to rapid development of leukemia and lymphoma. Cell 83: 289-299.
33. Abraham KM, Levin SD, Marth JD, Forbush KA, Perlmutter RM, (1991) Thymic tumorigenesis induced by overexpression of p56lck. Proc Natl Acad Sci U S A 88: 3977-3981.
34. Tremblay M, Tremblay CS, Herblot S, Aplan PD, Hebert J, et al. (2010) Modeling T-cell acute lymphoblastic leukemia induced by the SCL and LMO1 oncogenes. Genes Dev 24: 1093-1105.
35. Bain G, Engel I, Robanus Maandag EC, te Riele HP, Voland JR, et al. (1997) E2A deficiency leads to abnormalities in alphabeta T-cell development and to rapid development of T-cell lymphomas. Mol Cell Biol 17: 4782-4791.
36. Gothert JR, Brake RL, Smeets M, Duhrsen U, Begley CG, et al. (2007) NOTCH1 pathway activation is an early hallmark of SCL T leukemogenesis. Blood 110: 3753-3762.
37. Liu F, Walmsley M, Rodaway A, Patient R, (2008) Fli1 acts at the top of the transcriptional network driving blood and endothelial development. Curr Biol 18: 1234-1240.
38. Feng H, Stachura DL, White RM, Gutierrez A, Zhang L, et al. (2010) T-lymphoblastic lymphoma cells express high levels of BCL2, S1P1, and ICAM1, leading to a blockade of tumor cell intravasation. Cancer Cell 18: 353-366.
39. Engel I, Murre C, (2004) E2A proteins enforce a proliferation checkpoint in developing thymocytes. EMBO J 23: 202-211.
40. Armstrong SA, Look AT, (2005) Molecular genetics of acute lymphoblastic leukemia. J Clin Oncol 23: 6306-6315.
41. O'Neil J, Shank J, Cusson N, Murre C, Kelliher M, (2004) TAL1/SCL induces leukemia by inhibiting the transcriptional activity of E47/HEB. Cancer Cell 5: 587-596.
42. Palomero T, Odom DT, O'Neil J, Ferrando AA, Margolin A, et al. (2006) Transcriptional regulatory networks downstream of TAL1/SCL in T-cell acute lymphoblastic leukemia. Blood 108: 986-992.
43. Yashiro-Ohtani Y, He Y, Ohtani T, Jones ME, Shestova O, et al. (2009) Pre-TCR signaling inactivates Notch1 transcription by antagonizing E2A. Genes Dev 23: 1665-1676.
44. Nie L, Wu H, Sun XH, (2008) Ubiquitination and degradation of Tal1/SCL are induced by notch signaling and depend on Skp2 and CHIP. J Biol Chem 283: 684-692.
45. Miyazaki M, Rivera RR, Miyazaki K, Lin YC, Agata Y, et al. (2011) The opposing roles of the transcription factor E2A and its antagonist Id3 that orchestrate and enforce the naive fate of T cells. Nat Immunol 12: 992-1001.
46. Mercer EM, Lin YC, Benner C, Jhunjhunwala S, Dutkowski J, et al. (2011) Multilineage priming of enhancer repertoires precedes commitment to the B and myeloid cell lineages in hematopoietic progenitors. Immunity 35: 413-425.
47. Reschly EJ, Spaulding C, Vilimas T, Graham WV, Brumbaugh RL, et al. (2006) Notch1 promotes survival of E2A-deficient T cell lymphomas through pre-T cell receptor-dependent and-independent mechanisms. Blood 107: 4115-4121.
48. Heng TS, Painter MW, (2008) The Immunological Genome Project: networks of gene expression in immune cells. Nat Immunol 9: 1091-1094.
49. Wilson NK, Foster SD, Wang X, Knezevic K, Schutte J,et al. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 7: 532-544.
50. Haydu JE, De Keersmaecker K, Duff MK, Paietta E, Racevskis J, et al. (2012) An activating intragenic deletion in NOTCH1 in human T-ALL. Blood 119: 5211-5214.
51. Kamstrup MR, Ralfkiaer E, Skovgaard GL, Gniadecki R, (2008) Potential involvement of Notch1 signalling in the pathogenesis of primary cutaneous CD30-positive lymphoproliferative disorders. Br J Dermatol 158: 747-753.
52. Quick CM, Smoller BR, Hiatt KM, (2006) Fli-1 expression in mycosis fungoides. J Cutan Pathol 33: 642-645.
53. Folpe AL, Hill CE, Parham DM, O'Shea PA, Weiss SW, (2000) Immunohistochemical detection of FLI-1 protein expression: a study of 132 round cell tumors with emphasis on CD99-positive mimics of Ewing's sarcoma/primitive neuroectodermal tumor. Am J Surg Pathol 24: 1657-1662.
54. Mhawech-Fauceglia P, Herrmann FR, Bshara W, Odunsi K, Terracciano L, et al. (2007) Friend leukaemia integration-1 expression in malignant and benign tumours: a multiple tumour tissue microarray analysis using polyclonal antibody. J Clin Pathol 60: 694-700.
55. Grohar PJ, Woldemichael GM, Griffin LB, Mendoza A, Chen QR, et al. (2011) Identification of an inhibitor of the EWS-FLI1 oncogenic transcription factor by high-throughput screening. J Natl Cancer Inst 103: 962-978.
56. Li Y-J, Zhao X, Vecchiarelli-Federico LM, Li Y, Datti A, et al. (2012) Drug-mediated inhibition of Fli-1 for the treatment of leukemia. Blood Cancer Journal 2: 1-9.