AML1-ETO targets and suppresses cathepsin G, a serine protease, which is able to degrade AML1-ETO in t(8;21) acute myeloid leukemia

Oncogene

Volumn 32, Issue 15, 2013, Pages 1978-1987

  Jin, W ^a   Wu, K ^a   Li, Y Z ^a   Yang, W T ^a   Zou, B ^a   Zhang, F ^a   Zhang, J ^a,b   Wang, K K ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

AML1 ETO; cathepsin G; t(8; 21) AML

Indexed keywords

AML1 ETO PROTEIN; ANTINEOPLASTIC AGENT; CATHEPSIN G; LUCIFERASE; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; LEUKEMOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEGRADATION; REGULATORY MECHANISM; TRANSACTIVATION; WILD TYPE;

APOPTOSIS; CATHEPSIN G; CELL DIFFERENTIATION; CELL LINE, TUMOR; CORE BINDING FACTOR ALPHA 2 SUBUNIT; DNA-BINDING PROTEINS; DOWN-REGULATION; GENE EXPRESSION REGULATION, LEUKEMIC; HEK293 CELLS; HELA CELLS; HEMATOPOIESIS; HL-60 CELLS; HUMANS; IMMUNOLOGIC SURVEILLANCE; LEUKEMIA, MYELOID, ACUTE; ONCOGENE PROTEINS, FUSION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENES; TRANSCRIPTION FACTORS; TUMOR ESCAPE;

EID: 84876100193     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.204     Document Type: Article

References (51)

1. Peterson LF, Zhang DE. The 8;21 translocation in leukemogenesis. Oncogene 2004; 23: 4255-4262.
2. Licht JD. AML1 and the AML1-ETO fusion protein in the pathogenesis of t(8;21) AML. Oncogene 2001; 20: 5660-5679.
3. Frank R, Zhang J, Uchida H, Meyers S, Hiebert SW, Nimer SD. The AML1/ETO fusion protein blocks transactivation of the GM-CSF promoter by AML1B. Oncogene 1995; 11: 2667-2674.
4. Nuchprayoon I, Meyers S, Scott LM, Suzow J, Hiebert S, Friedman AD. PEBP2/CBF, the murine homolog of the human myeloid AML1 and PEBP2 beta/CBF beta proto-oncoproteins, regulates the murine myeloperoxidase and neutrophil elas-tase genes in immature myeloid cells. Mol Cell Biol 1994; 14: 5558-5568.
5. Uchida H, Zhang J, Nimer SD. AML1A and AML1B can transactivate the human IL-3 promoter. J Immunol 1997; 158: 2251-2258.
6. Hug BA, Lazar MA. ETO interacting proteins. Oncogene 2004; 23: 4270-4274.
7. Yergeau DA, Hetherington CJ, Wang Q, Zhang P, Sharpe AH, Binder M et al. Embryonic lethality and impairment of haematopoiesis in mice heterozygous for an AML1-ETO fusion gene. Nat Genet 1997; 15: 303-306.
8. Okuda T, Cai Z, Yang S, Lenny N, Lyu CJ, van Deursen JM et al. Expression of a knocked-in AML1-ETO leukemia gene inhibits the establishment of normal definitive hematopoiesis and directly generates dysplastic hematopoietic progenitors. Blood 1998; 91: 3134-3143.
9. Klampfer L, Zhang J, Zelenetz AO, Uchida H, Nimer SD. The AML1/ETO fusion protein activates transcription of BCL-2. Proc Natl Acad Sci USA 1996; 93: 14059-14064.
10. Traver D, Akashi K, Weissman IL, Lagasse E. Mice defective in two apoptosis pathways in the myeloid lineage develop acute myeloblastic leukemia. Immunity 1998; 9: 47-57.
11. Vangala RK, Heiss-Neumann MS, Rangatia JS, Singh SM, Schoch C, Tenen DG et al. The myeloid master regulator transcription factor PU.1 is inactivated by AML1-ETO in t(8;21) myeloid leukemia. Blood 2003; 101: 270-277.
12. McGhee L, Bryan J, Elliott L, Grimes HL, Kazanjian A, Davis JN et al. Gfi-1 attaches to the nuclear matrix, associates with ETO (MTG8) and histone deacetylase proteins, and represses transcription using a TSA-sensitive mechanism. J Cell Biochem 2003; 89: 1005-1018.
13. Westendorf JJ, Yamamoto CM, Lenny N, Downing JR, Selsted ME, Hiebert SW. The t(8;21) fusion product, AML-1-ETO, associates with C/EBP-alpha, inhibits C/EBP-alpha-dependent transcription, and blocks granulocytic differentiation. Mol Cell Biol 1998; 18: 322-333.
14. Higuchi M, O'Brien D, Kumaravelu P, Lenny N, Yeoh EJ, Downing JR. Expression of a conditional AML1-ETO oncogene bypasses embryonic lethality and establishes a murine model of human t(8;21) acute myeloid leukemia. Cancer Cell 2002; 1: 63-74.
15. Bitter MA, Le Beau MM, Rowley JD, Larson RA, Golomb HM, Vardiman JW. Associations between morphology, karyotype, and clinical features in myeloid leukemias. Hum Pathol 1987; 18: 211-225.
16. Pham CT. Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol 2006; 6: 541-550.
17. Dengler R, Munstermann U, al-Batran S, Hausner I, Faderl S, Nerl C et al. Immu-nocytochemical and flow cytometric detection of proteinase 3 (myeloblastin) in normal and leukaemic myeloid cells. Br J Haematol 1995; 89: 250-257.
18. Lausen J, Liu S, Fliegauf M, Lubbert M, Werner MH. ELA2 is regulated by hema-topoietic transcription factors, but not repressed by AML1-ETO. Oncogene 2006; 25: 1349-1357.
19. Mulloy JC, Jankovic V, Wunderlich M, Delwel R, Cammenga J, Krejci O et al. AML1-ETO fusion protein up-regulates TRKA mRNA expression in human CD34+ cells, allowing nerve growth factor-induced expansion. Proc Natl Acad Sci USA 2005; 102: 4016-4021.
20. Gardini A, Cesaroni M, Luzi L, Okumura AJ, Biggs JR, Minardi SP et al. AML1/ETO oncoprotein is directed to AML1 binding regions and co-localizes with AML1 and HEB on its targets. PLoS Genet 2008; 4: e1000275.
21. Dunne J, Cullmann C, Ritter M, Soria NM, Drescher B, Debernardi S et al. siRNA-mediated AML1/MTG8 depletion affects differentiation and proliferation-associated gene expression in t(8;21)-positive cell lines and primary AML blasts. Oncogene 2006; 25: 6067-6078.
22. Korkmaz B, Moreau T, Gauthier F. Neutrophil elastase, proteinase 3 and cathepsin G: physicochemical properties, activity and physiopathological functions. Biochimie 2008; 90: 227-242.
23. Piazza F, Valens J, Lagasse E, Schindler C. Myeloid differentiation of FdCP1 cells is dependent on Stat5 processing. Blood 2000; 96: 1358-1365.
24. Biggs JR, Yang J, Gullberg U, Muchardt C, Yaniv M, Kraft AS. The human brm protein is cleaved during apoptosis: the role of cathepsin G. Proc Natl Acad Sci USA 2001; 98: 3814-3819.
25. Shimada H, Ichikawa H, Ohki M. Potential involvement of the AML1-MTG8 fusion protein in the granulocytic maturation characteristic of the t(8;21) acute myelo-genous leukemia revealed by microarray analysis. Leukemia 2002; 16: 874-885.
26. Fliegauf M, Stock M, Berg T, Lubbert M. Williams-Beuren syndrome critical region-5/non-T-cell activation linker: a novel target gene of AML1/ETO. Oncogene 2004; 23: 9070-9081.
27. Lennartsson A, Garwicz D, Lindmark A, Gullberg U. The proximal promoter of the human cathepsin G gene conferring myeloid-specific expression includes C/EBP, c-myb and PU.1 binding sites. Gene 2005; 356: 193-202.
28. Linggi B, Muller-Tidow C, van de LL, Hu M, Nip J, Serve H et al. The t(8;21) fusion protein, AML1 ETO, specifically represses the transcription of the p14(ARF) tumor suppressor in acute myeloid leukemia. Nat Med 2002; 8: 743-750.
29. Wingender E. The TRANSFAC project as an example of framework technology that supports the analysis of genomic regulation. Brief Bioinform 2008; 9: 326-332.
30. Garwicz D, Lindmark A, Persson AM, Gullberg U. On the role of the proform-conformation for processing and intracellular sorting of human cathepsin G. Blood 1998; 92: 1415-1422.
31. Heidenreich O, Krauter J, Riehle H, Hadwiger P, John M, Heil G et al. AML1/MTG8 oncogene suppression by small interfering RNAs supports myeloid differentiation of t(8;21)-positive leukemic cells. Blood 2003; 101: 3157-3163.
32. Valk PJ, Verhaak RG, Beijen MA, Erpelinck CA, Barjesteh van Waalwijk van D-K, Boer JM et al. Prognostically useful gene-expression profiles in acute myeloid leukemia. N Engl J Med 2004; 350: 1617-1628.
33. Tomasson MH, Xiang Z, Walgren R, Zhao Y, Kasai Y, Miner T et al. Somatic mutations and germline sequence variants in the expressed tyrosine kinase genes of patients with de novo acute myeloid leukemia. Blood 2008; 111: 4797-4808.
34. Wouters BJ, Lowenberg B, Erpelinck-Verschueren CA, van Putten WL, Valk PJ, Delwel R. Double CEBPA mutations, but not single CEBPA mutations, define a subgroup of acute myeloid leukemia with a distinctive gene expression profile that is uniquely associated with a favorable outcome. Blood 2009; 113: 3088-3091.
35. Kadkol SS, Bruno A, Dodge C, Lindgren V, Ravandi F. Comprehensive analysis of CBFbeta-MYH11 fusion transcripts in acute myeloid leukemia by RT-PCR analysis. J Mol Diagn 2004; 6: 22-27.
36. Senyuk V, Sinha KK, Li D, Rinaldi CR, Yanamandra S, Nucifora G. Repression of RUNX1 activity by EVI1: a new role of EVI1 in leukemogenesis. Cancer Res 2007; 67: 5658-5666.
37. Mulloy JC, Cammenga J, MacKenzie KL, Berguido FJ, Moore MA, Nimer SD. The AML1-ETO fusion protein promotes the expansion of human hematopoietic stem cells. Blood 2002; 99: 15-23.
38. Mulloy JC, Cammenga J, Berguido FJ, Wu K, Zhou P, Comenzo RL et al. Maintaining the self-renewal and differentiation potential of human CD34 + hema-topoietic cells using a single genetic element. Blood 2003; 102: 4369-4376.
39. Igney FH, Krammer PH. Immune escape of tumors: apoptosis resistance and tumor counterattack. J Leukoc Biol 2002; 71: 907-920.
40. Howcroft TK, Weissman JD, Gegonne A, Singer DSA. T lymphocyte-specific transcription complex containing RUNX1 activates MHC class I expression. J Immunol 2005; 174: 2106-2115.
41. Okumura AJ, Peterson LF, Okumura F, Boyapati A, Zhang DE. t(8;21)(q22;q22) Fusion proteins preferentially bind to duplicated AML1/RUNX1 DNA-binding sequences to differentially regulate gene expression. Blood 2008; 112: 1392-1401.
42. Laricchia-Robbio L, Premanand K, Rinaldi CR, Nucifora G. EVI1 impairs myelopoi-esis by deregulation of PU.1 function. Cancer Res 2009; 69: 1633-1642.
43. Kitareewan S, Roebuck BD, Demidenko E, Sloboda RD, Dmitrovsky E. Lysosomes and trivalent arsenic treatment in acute promyelocytic leukemia. J Natl Cancer Inst 2007; 99: 41-52.
44. Puissant A, Colosetti P, Robert G, Cassuto JP, Raynaud S, Auberger P. Cathepsin B release after imatinib-mediated lysosomal membrane permeabilization triggers BCR-ABL cleavage and elimination of chronic myelogenous leukemia cells. Leukemia 2010; 24: 115-124.
45. Wang L, Zhao WL, Yan JS, Liu P, Sun HP, Zhou GB et al. Eriocalyxin B induces apoptosis of t(8;21) leukemia cells through NF-kappaB and MAPK signaling pathways and triggers degradation of AML1-ETO oncoprotein in a caspase-3-dependent manner. Cell Death Differ 2007; 14: 306-317.
46. Zhou GB, Kang H, Wang L, Gao L, Liu P, Xie J et al. Oridonin, a diterpenoid extracted from medicinal herbs, targets AML1-ETO fusion protein and shows potent antitumor activity with low adverse effects on t(8;21) leukemia in vitro and in vivo. Blood 2007; 109: 3441-3450.
47. Yang G, Thompson MA, Brandt SJ, Hiebert SW. Histone deacetylase inhibitors induce the degradation of the t(8;21) fusion oncoprotein. Oncogene 2007 26: 91-101.
48. Jiang Y, Xue ZH, Shen WZ, Du KM, Yan H, Yu Y et al. Desferrioxamine induces leukemic cell differentiation potentially by hypoxia-inducible factor-1 alpha that augments transcriptional activity of CCAAT/enhancer-binding protein-alpha. Leukemia 2005; 19: 1239-1247.
49. Wang K, Wang P, Shi J, Zhu X, He M, Jia X et al. PML/RARalpha targets promoter regions containing PU.1 consensus and RARE half sites in acute promyelocytic leukemia. Cancer Cell 2010; 17: 186-197.
50. Lane AA, Ley TJ. Neutrophil elastase cleaves PML-RARalpha and is important for the development of acute promyelocytic leukemia in mice. Cell 2003; 115: 305-318.
51. Corsello SM, Roti G, Ross KN, Chow KT, Galinsky I, DeAngelo DJ et al. Identification of AML1-ETO modulators by chemical genomics. Blood 2009; 113: 6193-6205.