Lack of the p42 form of C/EBPα leads to spontaneous immortalization and lineage infidelity of committed myeloid progenitors

Experimental Hematology

Volumn 41, Issue 10, 2013, Pages 882-893.e16

  Schuster, Mikkel B ^a,b   Frank, Anne Katrine ^a,b   Bagger, Frederik O ^a,b,c   Rapin, Nicolas ^a,b,c   Vikesaa, Jonas ^d   Porse, Bo T ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d Rigshospitalet   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; PROTEIN P42;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL IMMORTALIZATION; CELL LINEAGE; CELL RENEWAL; CELL TRANSFORMATION; CLONAL VARIATION; COLONY FORMING UNIT GM; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

EID: 84885692432     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2013.06.003     Document Type: Article

References (48)

1. Dick J.E. Stem cell concepts renew cancer research. Blood 2008, 112:4793-4807.
2. Jan M., Snyder T.M., Corces-Zimmerman M.R., et al. Clonal evolution of preleukemic hematopoietic stem cells precedes human acute myeloid leukemia. Sci Transl Med 2012, 4:149ra118.
3. Lapidot T., Sirard C., Vormoor J., et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
4. Blair A., Hogge D.E., Ailles L.E., Lansdorp P.M., Sutherland H.J. Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability invitro and invivo. Blood 1997, 89:3104-3112.
5. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997, 3:730-737.
6. Ishikawa F., Yoshida S., Saito Y., et al. Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nat Biotechnol 2007, 25:1315-1321.
7. Tan B.T., Park C.Y., Ailles L.E., Weissman I.L. The cancer stem cell hypothesis: A work in progress. Lab Invest 2006, 86:1203-1207.
8. Taussig D.C., Miraki-Moud F., Anjos-Afonso F., et al. Anti-CD38 antibody-mediated clearance of human repopulating cells masks theheterogeneity of leukemia-initiating cells. Blood 2008, 112:568-575.
9. Turhan A.G., Lemoine F.M., Debert C., et al. Highly purified primitive hematopoietic stem cells are PML-RARA negative and generate nonclonal progenitors in acute promyelocytic leukemia. Blood 1995, 85:2154-2161.
10. Huntly B.J., Shigematsu H., Deguchi K., et al. MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell 2004, 6:587-596.
11. Ayton P.M., Cleary M.L. Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev 2003, 17:2298-2307.
12. Cozzio A., Passegue E., Ayton P.M., Karsunky H., Cleary M.L., Weissman I.L. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev 2003, 17:3029-3035.
13. Krivtsov A.V., Twomey D., Feng Z., et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 2006, 442:818-822.
14. Radomska H.S., Huettner C.S., Zhang P., Cheng T., Scadden D.T., Tenen D.G. CCAAT/enhancer binding protein alpha is a regulatory switch sufficient for induction of granulocytic development from bipotential myeloid progenitors. Mol Cell Biol 1998, 18:4301-4314.
15. Wang X., Scott E., Sawyers C.L., Friedman A.D. C/EBPalpha bypasses granulocyte colony-stimulating factor signals to rapidly induce PU.1 gene expression, stimulate granulocytic differentiation, and limit proliferation in 32D cl3 myeloblasts. Blood 1999, 94:560-571.
16. Iwama A., Osawa M., Hirasawa R., et al. Reciprocal roles for CCAAT/enhancer binding protein (C/EBP) and PU.1 transcription factors in Langerhans cell commitment. J Exp Med 2002, 195:547-558.
17. Zhang D.E., Zhang P., Wang N.D., Hetherington C.J., Darlington G.J., Tenen D.G. 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.
18. Zhang P., Iwama A., Datta M.W., Darlington G.J., Link D.C., Tenen D.G. Upregulation of interleukin 6 and granulocyte colony-stimulating factor receptors by transcription factor CCAAT enhancer binding protein alpha (C/EBP alpha) is critical for granulopoiesis. J Exp Med 1998, 188:1173-1184.
19. Heath V., Suh H.C., Holman M., et al. C/EBPalpha deficiency results in hyperproliferation of hematopoietic progenitor cells and disrupts macrophage development invitro and invivo. Blood 2004, 104:1639-1647.
20. Schuster M.B., Porse B.T. C/EBPalpha: A tumour suppressor in multiple tissues?. Biochim Biophys Acta 2006, 1766:88-103.
21. 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.
22. Fazi F., Rosa A., Fatica A., et al. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 2005, 123:819-831.
23. Porse B.T., Bryder D., Theilgaard-Monch K., et al. Loss of C/EBP alphacell cycle control increases myeloid progenitor proliferation and transforms the neutrophil granulocyte lineage. J Exp Med 2005, 202:85-96.
24. Porse B.T., Pedersen T.A., Xu X., et al. E2F repression by C/EBPalpha is required for adipogenesis and granulopoiesis invivo. Cell 2001, 107:247-258.
25. Schuster M.B., Porse B.T. C/EBPalpha in leukemogenesis: Identity and origin of the leukemia-initiating cell. Biofactors 2009, 35:227-231.
26. Lin L.I., Chen C.Y., Lin D.T., et al. Characterization of CEBPA mutations in acute myeloid leukemia: most patients with CEBPA mutations have biallelic mutations and show a distinct immunophenotype of the leukemic cells. Clin Cancer Res 2005, 11:1372-1379.
27. Tiesmeier J., Czwalinna A., Muller-Tidow C., et al. Evidence for allelic evolution of C/EBPalpha mutations in acute myeloid leukaemia. Br J Haematol 2003, 123:413-419.
28. Leroy H., Roumier C., Huyghe P., Biggio V., Fenaux P., Preudhomme C. CEBPA point mutations in hematological malignancies. Leukemia 2005, 19:329-334.
29. Nerlov C. C/EBPalpha mutations in acute myeloid leukaemias. Nat Rev Cancer 2004, 4:394-400.
30. Kirstetter P., Schuster M.B., Bereshchenko O., et al. Modeling of C/EBPalpha mutant acute myeloid leukemia reveals a common expression signature of committed myeloid leukemia-initiating cells. Cancer Cell 2008, 13:299-310.
31. Bereshchenko O., Mancini E., Moore S., et al. Hematopoietic stem cell expansion precedes the generation of committed myeloid leukemia-initiating cells in C/EBPalpha mutant AML. Cancer Cell 2009, 16:390-400.
32. Wouters B.J., Jorda M.A., Keeshan K., et al. Distinct gene expression profiles of acute myeloid/T-lymphoid leukemia with silenced CEBPA and mutations in NOTCH1. Blood 2007, 110:3706-3714.
33. Figueroa M.E., Wouters B.J., Skrabanek L., et al. Genome-wide epigenetic analysis delineates a biologically distinct immature acute leukemia with myeloid/T-lymphoid features. Blood 2009, 113:2795-2804.
34. Wouters B.J., Lowenberg B., Erpelinck-Verschueren C.A., van Putten W.L., Valk P.J., 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. Pronk C.J., Rossi D.J., Mansson R., et al. Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell 2007, 1:428-442.
36. Adolfsson J., Mansson R., Buza-Vidas N., et al. Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 2005, 121:295-306.
37. Doulatov S., Notta F., Eppert K., Nguyen L.T., Ohashi P.S., Dick J.E. Revised map of the human progenitor hierarchy shows the origin of macrophages and dendritic cells in early lymphoid development. Nat Immunol 2010, 11:585-593.
38. Kohn L.A., Hao Q.L., Sasidharan R., et al. Lymphoid priming in human bone marrow begins before expression of CD10 with upregulation of L-selectin. Nat Immunol 2012, 13:963-971.
39. Ng S.Y., Yoshida T., Zhang J., Georgopoulos K. Genome-wide lineage-specific transcriptional networks underscore Ikaros-dependent lymphoid priming in hematopoietic stem cells. Immunity 2009, 30:493-507.
40. Bell J.J., Bhandoola A. The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 2008, 452:764-767.
41. Wada H., Masuda K., Satoh R., et al. Adult T-cell progenitors retain myeloid potential. Nature 2008, 452:768-772.
42. Wolfler A., Danen-van Oorschot A.A., Haanstra J.R., et al. Lineage-instructive function of C/EBPalpha in multipotent hematopoietic cells and early thymic progenitors. Blood 2010, 116:4116-4125.
43. Laiosa C.V., Stadtfeld M., Xie H., de Andres-Aguayo L., Graf T. Reprogramming of committed T cell progenitors to macrophages and dendritic cells by C/EBP alpha and PU.1 transcription factors. Immunity 2006, 25:731-744.
44. Hollink I.H., van den Heuvel-Eibrink M.M., Arentsen-Peters S.T., et al. Characterization of CEBPA mutations and promoter hypermethylation in pediatric acute myeloid leukemia. Haematologica 2011, 96:384-392.
45. Keeshan K., He Y., Wouters B.J., et al. Tribbles homolog 2 inactivates C/EBPalpha and causes acute myelogenous leukemia. Cancer Cell 2006, 10:401-411.
46. Cantor A.B., Orkin S.H. Hematopoietic development: A balancing act. Curr Opin Genet Dev 2001, 11:513-519.
47. Chang H.C., Han L., Jabeen R., Carotta S., Nutt S.L., Kaplan M.H. PU.1 regulates TCR expression by modulating GATA-3 activity. J Immunol 2009, 183:4887-4894.
48. Querfurth E., Schuster M., Kulessa H., et al. Antagonism between C/EBPbeta and FOG in eosinophil lineage commitment of multipotent hematopoietic progenitors. Genes Dev 2000, 14:2515-2525.