High levels of the BCR/ABL oncoprotein are required for the MAPK-hnRNP-E2-dependent suppression of C/EBPα-driven myeloid differentiation

Blood

Volumn 110, Issue 3, 2007, Pages 994-1003

  Ji, Suk Chang ^a   Santhanam, Ramasamy ^a   Trotta, Rossana ^a   Neviani, Paolo ^a   Eiring, Anna M ^a   Briercheck, Edward ^a   Ronchetti, Mattia ^b   Roy, Denis C ^c   Calabretta, Bruno ^b   Caligiuri, Michael A ^a   Perrotti, Danilo ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MONTREAL   (Canada)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CCAAT ENHANCER BINDING PROTEIN ALPHA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ARTICLE; BLAST CELL CRISIS; BONE MARROW CELL; CELL DIFFERENTIATION; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; GENE DOSAGE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NEUTROPHIL; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UNTRANSLATED REGION;

EID: 34547958804     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-03-078303     Document Type: Article

References (70)

1. Calabretta B, Perrotti D. The biology of CML blast crisis. Blood. 2004;103:4010-4022.
2. Tenen DG, Hromas R, Licht JD, Zhang DE. Transcription factors, normal myeloid development, and leukemia. Blood. 1997;90:489-519.
3. Ward AC, Loeb DM, Soede-Bobok AA, Touw IP, Friedman AD. Regulation of granulopoiesis by transcription factors and cytokine signals. Leukemia. 2000;14:973-990.
4. Cheng T, Shen H, Giokas D, Gere J, Tenen DG, Scadden DT. Temporal mapping of gene expression levels during the differentiation of individual primary hematopoietic cells. Proc Natl Acad Sci U S A. 1996;93:13158-13163.
5. Zhang DE, Zhang P, Wang ND, Hetherington CJ, Darlington GJ, Tenen DG. Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein alpha-deficient mice. Proc Natl Acad Sci U S A. 1997;94:569-574.
6. Zhang P, Iwasaki-Arai J, Iwasaki H, et al. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBP alpha. Immunity. 2004;21:853-863.
7. Smith LT, Hohaus S, Gonzalez DA, Dziennis SE, Tenen DG. PU.1 (Spi-1) and C/EBP alpha regulate the granulocyte colony-stimulating factor receptor promoter in myeloid cells. Blood. 1996;88:1234-1247.
8. Ford AM, Bennett CA, Healy LE, Towatari M, Greaves MF, Enver T. Regulation of the myeloperoxidase enhancer binding proteins Pu1, C-EBP alpha, -beta, and -delta during granulocyte-lineage specification. Proc Natl Acad Sci U S A. 1996;93:10838-10843.
9. Oelgeschlager M, Nuchprayoon I, Luscher B, Friedman AD. C/EBP, c-Myb, and PU. 1 cooperate to regulate the neutrophil elastase promoter. Mol Cell Biol. 1996;16:4717-4725.
10. Keeshan K, Santilli G, Corradini F, Perrotti D, Calabretta B. Transcription activation function of C/EBPalpha is required for induction of granulocytic differentiation. Blood. 2003;102:1267-1275.
11. Perrotti D, Cesi V, Trotta R, Guerzoni C, et al. BCR-ABL suppresses C/EBPalpha expression through inhibitory action of hnRNP E2. Nat Genet. 2002;30:48-58.
12. Schuster C, Forster K, Dierks H, et al. The effects of Bcr-Abl on C/EBP transcription-factor regulation and neutrophilic differentiation are reversed by the Abl kinase inhibitor imatinib mesylate. Blood. 2003;101:655-663.
13. Tavor S, Park DJ, Gery S, Vuong PT, Gombart AF, Koeffler HP. Restoration of C/EBPalpha expression in a BCR-ABL+ cell line induces terminal granulocytic differentiation. J Biol Chem. 2003;278:52651-52659.
14. Ferrari-Amorotti G, Keeshan K, Zattoni M, et al. Leukemogenesis induced by wild-type and STI571-resistant BCR/ABL is potently suppressed by C/EBPalpha. Blood. 2006;108:1353-1362.
15. Wagner K, Zhang P, Rosenbauer F, et al. Absence of the transcription factor CCAAT enhancer binding protein alpha results in loss of myeloid identity in bcr/abl-induced malignancy. Proc Natl Acad Sci U S A. 2006;103:6338-6343.
16. Perrotti D, Marcucci G, Caligiuri MA. Loss of C/EBP alpha and favorable prognosis of acute myeloid leukemias: a biological paradox. J Clin Oncol. 2004;22:582-584.
17. Tenen DG. Disruption of differentiation in human cancer: AML shows the way. Nat Rev Cancer. 2003;3:89-101.
18. Pabst T, Mueller BU, Zhang P, et al. Dominant-negative mutations of CEBPA, encoding CCAAT/enhancer binding protein-alpha (C/EBPalpha), in acute myeloid leukemia. Nat Genet. 2001;27:263-270.
19. Gombart AF, Hofmann WK, Kawano S, et al. Mutations in the gene encoding the transcription factor CCAAT/enhancer binding protein alpha in myelodysplastic syndromes and acute myeloid leukemias. Blood. 2002;99:1332-1340.
20. Pabst T, Stillner E, Neuberg D, et al. Mutations of the myeloid transcription factor CEBPA are not associated with the blast crisis of chronic myeloid leukaemia. Br J Haematol. 2006;133:400-402.
21. Notari M, Neviani P, Santhanam R, et al. A MAPK/HNRPK pathway controls BCR/ABL oncogenic potential by regulating MYC mRNA translation. Blood. 2006;107:2507-2516.
22. Thomson AM, Rogers JT, Walker CE, Staton JM, Leedman PJ. Optimized RNA gel-shift and UV cross-linking assays for characterization of cytoplasmic RNA-protein interactions. BioTechniques. 1999;27:1032-1039, 1042.
23. Neviani P, Santhanam R, Trotta R, et al. The tumor suppressor PP2A is functionally inactivated in blast crisis CML through the inhibitory activity of the BCR/ABL-regulated SET protein. Cancer Cell. 2005;8:355-368.
24. Sebolt-Leopold JS, Dudley DT, Herrera R, et al. Blockade of the MAP kinase pathway suppresses growth of colon tumors in vivo. Nat Med. 1999;5:810-816.
25. Konopleva M, Shi Y, Steelman LS, et al. Development of a conditional in vivo model to evaluate the efficacy of small molecule inhibitors for the treatment of Raf-transformed hematopoietic cells. Cancer Res. 2005;65:9962-9970.
26. Tamura M, Orita T, Oh-eda M, et al. Reduction of the leukemogenic potential of malignant murine leukemic cells by in vivo treatment with recombinant human granulocyte colony-stimulating factor. Leuk Res. 1993;17:593-600.
27. Pospisil M, Hofer M, Znojil V, Vacha J, Netikova J, Hola J. Synergistic effect of granulocyte colony-stimulating factor and drugs elevating extracellular adenosine on neutrophil production in mice. Blood. 1995;86:3692-3697.
28. Makeyev AV, Chkheidze AN, Liebhaber SA. A set of highly conserved RNA-binding proteins, alphaCP-1 and alphaCP-2, implicated in mRNA stabilization, are coexpressed from an intronless gene and its intron-containing paralog. J Biol Chem. 1999;274:24849-24857.
29. Gotoh A, Miyazawa K, Ohyashiki K, Toyama K. Potential molecules implicated in downstream signaling pathways of p185BCR-ABL in Ph+ALL involve GTPase-activating protein, phospholipase C-gamma 1, and phosphatidylinositol 3′-kinase. Leukemia. 1994;8:115-120.
30. Matulonis U, Salgia R, Okuda K, Druker B, Griffin JD. Interleukin-3 and p210 BCR/ABL activate both unique and overlapping pathways of signal transduction in a factor-dependent myeloid cell line. Exp Hematol. 1993;21:1460-1466.
31. Goga A, McLaughlin J, Afar DE, Saffran DC, Witte ON. Alternative signals to RAS for hematopoietic transformation by the BCR-ABL oncogene. Cell. 1995;82:981-988.
32. Skorski T, Bellacosa A, Nieborowska-Skorska M, et al. Transformation of hematopoietic cells by BCR/ABL requires activation of a PI-3k/Akt-dependent pathway. EMBO J. 1997;16:6151-6161.
33. Carlesso N, Frank DA, Griffin JD. Tyrosyl phosphorylation and DNA binding activity of signal transducers and activators of transcription (STAT) proteins in hematopoietic cell lines transformed by Bcr/Abl. J Exp Med. 1996;183:811-820.
34. Cheng M, Wang D, Roussel MF. Expression of c-Myc in response to colony-stimulating factor-1 requires mitogen-activated protein kinase kinase-1. J Biol Chem. 1999;274:6553-6558.
35. Gonzalez FA, Raden DL, Davis RJ. Identification of substrate recognition determinants for human ERK1 and ERK2 protein kinases. J Biol Chem. 1991;266:22159-22163.
36. Davis RJ. The mitogen-activated protein kinase signal transduction pathway. J Biol Chem. 1993;268:14553-14556.
37. Allen LF, Sebolt-Leopold J, Meyer MB. CI-1040 (PD184352), a targeted signal transduction inhibitor of MEK (MAPKK). Semin Oncol. 2003;30:105-116.
38. Klein PJ, Schmidt CM, Wiesenauer CA, et al. The effects of a novel MEK inhibitor PD184161 on MEK-ERK signaling and growth in human liver cancer. Neoplasia. 2006;8:1-8.
39. Sebolt-Leopold JS. MEK inhibitors: a therapeutic approach to targeting the Ras-MAP kinase pathway in tumors. Curr Pharm Des. 2004;10:1907-1914.
40. Sebolt-Leopold JS, English JM. Mechanisms of drug inhibition of signalling molecules. Nature. 2006;441:457-462.
41. Feinstein E, Cimino G, Gale RP, et al. p53 in chronic myelogenous leukemia in acute phase. Proc Natl Acad Sci U S A. 1991;88:6293-6297.
42. Trotta R, Vignudelli T, Candini O, et al. BCR/ABL activates mdm2 mRNA translation via the La antigen. Cancer Cell. 2003;3:145-160.
43. Yoon K, Smart RC. C/EBPalpha is a DNA damage-inducible p53-regulated mediator of the G1 checkpoint in keratinocytes. Mol Cell Biol. 2004;24:10650-10660.
44. Pierce A, Spooncer E, Wooley S, et al. Bcr-Abl protein tyrosine kinase activity induces a loss of p53 protein that mediates a delay in myeloid differentiation. Oncogene. 2000;19:5487-5497.
45. Skorski T, Nieborowska-Skorska M, Wlodarski P, et al. Blastic transformation of p53-deficient bone marrow cells by p210bcr/abl tyrosine kinase. Proc Natl Acad Sci U S A. 1996;93:13137-13142.
46. Perrotti D, Neviani P. ReSETting PP2A tumour suppressor activity in blast crisis and imatinib-resistant chronic myelogenous leukaemia. Br J Cancer. 2006;95:775-781.
47. Gaiger A, Henn T, Horth E, et al. Increase of bcr-abl chimeric mRNA expression in tumor cells of patients with chronic myeloid leukemia precedes disease progression. Blood. 1995;86:2371-2378.
48. Elmaagacli AH, Beelen DW, Opalka B, Seeber S, Schaefer UW. The amount of BCR-ABL fusion transcripts detected by the real-time quantitative polymerase chain reaction method in patients with Philadelphia chromosome positive chronic myeloid leukemia correlates with the disease stage. Ann Hematol. 2000;79:424-431.
49. Moravcova J, Zmekova V, Klamova H, et al. Differences and similarities in kinetics of BCR-ABL transcript levels in CML patients treated with imatinib mesylate for chronic or accelerated disease phase. Leuk Res. 2004;28:415-419.
50. Barnes DJ, Schultheis B, Adedeji S, Melo JV. Dose-dependent effects of Bcr-Abl in cell line models of different stages of chronic myeloid leukemia. Oncogene. 2005;24:6432-6440.
51. Schultheis B, Szydlo R, Mahon FX, Apperley JF, Melo JV. Analysis of total phosphotyrosine levels in CD34+ cells from CML patients to predict the response to imatinib mesylate treatment. Blood. 2005;105:4893-4894.
52. Jamieson CH, Ailles LE, Dylla SJ, et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med. 2004;351:657-667.
53. Guo JQ, Wang JY, Arlinghaus RB. Detection of BCR-ABL proteins in blood cells of benign phase chronic myelogenous leukemia patients. Cancer Res. 1991;51:3048-3051.
54. Perrotti D, Turturro F, Neviani P. BCR/ABL, mRNA translation and apoptosis. Cell Death Differ. 2005;12:534-540.
55. Iervolino A, Santilli G, Trotta R, et al. hnRNP A1 nucleocytoplasmic shuttling activity is required for normal myelopoiesis and BCR/ABL leukemogenesis. Mol Cell Biol. 2002;22:2255-2266.
56. Guerzoni C, Bardini M, Mariani SA, et al. Inducible activation of C/EBP{beta}, a gene negatively regulated by BCR/ABL, inhibits proliferation and promotes differentiation of BCR/ABL-expressing cells. Blood. 2006;107:4080-4089.
57. Perrotti D, Bonatti S, Trotta R, et al. TLS/FUS, a pro-oncogene involved in multiple chromosomal translocations, is a novel regulator of BCR/ABL-mediated leukemogenesis. EMBO J. 1998;17:4442-4455.
58. Perrotti D, Iervolino A, Cesi V, et al. BCR-ABL prevents c-jun-mediated and proteasome-dependent FUS (TLS) proteolysis through a protein kinase CbetaII-dependent pathway. Mol Cell Biol. 2000;20:6159-6169.
59. Yu C, Dasmahapatra G, Dent P, Grant S. Synergistic interactions between MEK1/2 and histone deacetylase inhibitors in BCR/ABL+ human leukemia cells. Leukemia. 2005;19:1579-1589.
60. Yu C, Krystal G, Varticovksi L, McKinstry R, et al. Pharmacologic mitogen-activated protein/extracellular signal-regulated kinase kinase/mitogenactivated protein kinase inhibitors interact synergistically with STI571 to induce apoptosis in Bcr/Abl-expressing human leukemia cells. Cancer Res. 2002;62:188-199.
61. Chu S, Holtz M, Gupta M, Bhatia R. BCR/ABL kinase inhibition by imatinib mesylate enhances MAP kinase activity in chronic myelogenous leukemia CD34+ cells. Blood. 2004;103:3167-3174.
62. Makeyev AV, Liebhaber SA. The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms. RNA. 2002;8:265-278.
63. Evans JR, Mitchell SA, Spriggs KA, et al. Members of the poly (rC) binding protein family stimulate the activity of the c-myc internal ribosome entry segment in vitro and in vivo. Oncogene. 2003;22:8012-8020.
64. Johansen LM, Iwama A, Lodie TA, et al. c-Myc is a critical target for c/EBPalpha in granulopoiesis. Mol Cell Biol. 2001;21:3789-3806.
65. Porse BT, Pedersen TA, Xu X, et al. E2F repression by C/EBPalpha is required for adipogenesis and granulopoiesis in vivo. Cell. 2001;107:247-258.
66. Holt JT, Redner RL, Nienhuis AW. An oligomer complementary to c-myc mRNA inhibits proliferation of HL-60 promyelocytic cells and induces differentiation. Mol Cell Biol. 1988;8:963-973.
67. Hoffman-Liebermann B, Liebermann DA. Suppression of c-myc and c-myb is tightly linked to terminal differentiation induced by IL6 or LIF and not growth inhibition in myeloid leukemia cells. Oncogene. 1991;6:903-909.
68. Samanta AK, Lin H, Sun T, Kantarjian H, Arlinghaus RB. Janus kinase 2: a critical target in chronic myelogenous leukemia. Cancer Res. 2006;66:6468-6472.
69. Ross SE, Radomska HS, Wu B, et al. Phosphorylation of C/EBPalpha inhibits granulopoiesis. Mol Cell Biol. 2004;24:675-686.
70. Radomska HS, Basseres DS, Zheng R, et al. Block of C/EBP alpha function by phosphorylation in acute myeloid leukemia with FLT3 activating mutations. J Exp Med. 2006;203:371-381.