The shortest isoform of C/EBPb, liver inhibitory protein (LIP), collaborates with Evi1 to induce AML in a mouse BMT model

Blood

Volumn 121, Issue 20, 2013, Pages 4142-4155

  Watanabe Okochi, Naoko ^a,b   Yoshimi, Akihide ^a   Sato, Tomohiko ^a   Ikeda, Toshiyuki ^b   Kumano, Keiki ^a   Taoka, Kazuki ^a   Satoh, Yumiko ^c   Shinohara, Akihito ^a   Tsuruta, Takako ^a   Masuda, Akiko ^c   Yokota, Hiromitsu ^c   Yatomi, Yutaka ^c   Takahashi, Koki ^b   Kitaura, Jiro ^d   Kitamura, Toshio ^d   Kurokawa, Mineo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b University of Tokushima   (Japan)

^c Department of Clinical Laboratory ^*  (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; ISOPROTEIN; LIVER INHIBITORY PROTEIN; PROTEIN; UNCLASSIFIED DRUG; CEBPB PROTEIN, MOUSE; DNA BINDING PROTEIN; EVI1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ACUTE MYELOID LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; CONTROLLED STUDY; EVI1 GENE; GENE; GENE OVEREXPRESSION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; WESTERN BLOTTING; ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; CELL CULTURE; CELL TRANSFORMATION; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; PROTO ONCOGENE;

ANIMALS; BONE MARROW TRANSPLANTATION; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PROTEIN ISOFORMS; PROTO-ONCOGENES; TRANSCRIPTION FACTORS;

MLCS; MLOWN;

EID: 84880992553     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-07-368654     Document Type: Article

References (51)

1. Lugthart S, van Drunen E, van Norden Y, et al. High EVI1 levels predict adverse outcome in acute myeloid leukemia: prevalence of EVI1 overexpression and chromosome 3q26 abnormalities underestimated. Blood. 2008; 111(8):4329-4337.
2. Groschel S, Lugthart S, Schlenk RF, et al. High EVI1 expression predicts outcome in younger adult patients with acute myeloid leukemia and is associated with distinct cytogenetic abnormalities. J Clin Oncol. 2010;28(12):2101-2107.
3. Kataoka K, Kurokawa M. Ecotropic viral integration site 1, stem cell self-renewal and leukemogenesis. Cancer Sci. 2012;103(8): 1371-1377.
4. Morishita K, Parker DS, Mucenski ML, Jenkins NA, Copeland NG, Ihle JN. Retroviral activation of a novel gene encoding a zinc finger protein in IL-3-dependent myeloid leukemia cell lines. Cell. 1988;54(6):831-840.
5. Calmels B, Ferguson C, Laukkanen MO, et al. Recurrent retroviral vector integration at the Mds1/Evi1 locus in nonhuman primate hematopoietic cells. Blood. 2005;106(7): 2530-2533.
6. Stein S, Ott MG, Schultze-Strasser S, et al. Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat Med. 2010;16(2):198-204.
7. Watanabe-Okochi N, Kitaura J, Ono R, et al. AML1 mutations induced MDS and MDS/AML in a mouse BMT model. Blood. 2008;111(8): 4297-4308.
8. Yoshimi A, Goyama S, Watanabe-Okochi N, et al. Evi1 represses PTEN expression and activates PI3K/AKT/mTOR via interactions with polycomb proteins. Blood. 2011;117(13):3617-3628.
9. Akira S, Isshiki H, Sugita T, et al. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 1990;9(6):1897-1906.
10. Akagi K, Suzuki T, Stephens RM, Jenkins NA, Copeland NG. RTCGD: retroviral tagged cancer gene database. Nucleic Acids Res. 2004; 32(Database issue):D523-D527.
11. Kajimura S, Seale P, Kubota K, et al. Initiation of myoblast to brown fat switch by a PRDM16-C/EBP-beta transcriptional complex. Nature. 2009; 460(7259):1154-1158.
12. Sanuki S, Hamanaka S, Kaneko S, et al. A new red fluorescent protein that allows efficient marking of murine hematopoietic stem cells. J Gene Med. 2008;10(9):965-971.
13. Morita S, Kojima T, Kitamura T. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 2000;7(12): 1063-1066.
14. Kitamura T, Koshino Y, Shibata F, et al. Retrovirus-mediated gene transfer and expression cloning: powerful tools in functional genomics. Exp Hematol. 2003;31(11):1007-1014.
15. Kogan SC, Ward JM, Anver MR, et al; Hematopathology subcommittee of the Mouse Models of Human Cancers Consortium. Bethesda proposals for classification of nonlymphoid hematopoietic neoplasms in mice. Blood. 2002; 100(1):238-245.
16. Baum C, editor. Genetic Modification of Hematopoietic Stem Cells. Methods in Molecular Biology: Methods and Protocols. Vol 506. New York, NY: Humana Press; 2009.
17. Riley J, Butler R, Ogilvie D, et al. A novel, rapid method for the isolation of terminal sequences from yeast artificial chromosome (YAC) clones. Nucleic Acids Res. 1990;18(10):2887-2890.
18. Arnold C, Hodgson IJ. Vectorette PCR: a novel approach to genomic walking. PCR Methods Appl. 1991;1(1):39-42.
19. Sterneck E, Zhu S, Ramirez A, Jorcano JL, Smart RC. Conditional ablation of C/EBP beta demonstrates its keratinocyte-specific requirement for cell survival and mouse skin tumorigenesis. Oncogene. 2006;25(8): 1272-1276.
20. Kuhn R, Schwenk F, Aguet M, Rajewsky K. Inducible gene targeting in mice. Science. 1995; 269(5229):1427-1429.
21. Watanabe-Okochi N, Oki T, Komeno Y, et al. Possible involvement of RasGRP4 in leukemogenesis. Int J Hematol. 2009;89(4): 470-481.
22. Goyama S, Yamamoto G, Shimabe M, et al. Evi-1 is a critical regulator for hematopoietic stem cells and transformed leukemic cells. Cell Stem Cell. 2008;3(2):207-220.
23. Ishibashi J, Firtina Z, Rajakumari S, et al. An Evi1-C/EBPb complex controls peroxisome proliferator-activated receptor g2 gene expression to initiate white fat cell differentiation. Mol Cell Biol. 2012;32(12):2289-2299.
24. Yuasa H, Oike Y, Iwama A, et al. Oncogenic transcription factor Evi1 regulates hematopoietic stem cell proliferation through GATA-2 expression. EMBO J. 2005;24(11):1976-1987.
25. Shimabe M, Goyama S, Watanabe-Okochi N, et al. Pbx1 is a downstream target of Evi-1 in hematopoietic stem/progenitors and leukemic cells. Oncogene. 2009;28(49):4364-4374.
26. 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 USA. 2006;103(16): 6338-6343.
27. Akasaka T, Balasas T, Russell LJ, et al. Five members of the CEBP transcription factor family are targeted by recurrent IGH translocations in B-cell precursor acute lymphoblastic leukemia (BCP-ALL). Blood. 2007;109(8):3451-3461.
28. Pal R, Janz M, Galson DL, et al. C/EBPbeta regulates transcription factors critical for proliferation and survival of multiple myeloma cells. Blood. 2009;114(18):3890-3898.
29. Haas SC, Huber R, Gutsch R, et al. ITD-and FL-induced FLT3 signal transduction leads to increased C/EBPbeta-LIP expression and LIP/LAP ratio by different signalling modules. Br J Haematol. 2010;148(5):777-790.
30. Duprez E, Wagner K, Koch H, Tenen DG. C/EBPbeta: a major PML-RARA-responsive gene in retinoic acid-induced differentiation of APL cells. EMBO J. 2003;22(21):5806-5816.
31. Descombes P, Schibler U. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell. 1991; 67(3):569-579.
32. Calkhoven CF, Muller C, Leutz A. Translational control of C/EBPalpha and C/EBPbeta isoform expression. Genes Dev. 2000;14(15):1920-1932.
33. Ossipow V, Descombes P, Schibler U. CCAAT/enhancer-binding protein mRNA is translated into multiple proteins with different transcription activation potentials. Proc Natl Acad Sci USA. 1993;90(17):8219-8223.
34. Akagi T, Saitoh T, O'Kelly J, Akira S, Gombart AF, Koeffler HP. Impaired response to GM-CSF and G-CSF, and enhanced apoptosis in C/EBPbetadeficient hematopoietic cells. Blood. 2008;111(6): 2999-3004.
35. Mueller BU, Pabst T, Fos J, et al. ATRA resolves the differentiation block in t(15;17) acute myeloid leukemia by restoring PU.1 expression. Blood. 2006;107(8):3330-3338.
36. Rosenbauer F, Tenen DG. Transcription factors in myeloid development: balancing differentiation with transformation. Nat Rev Immunol. 2007;7(2): 105-117.
37. Kirstetter P, Schuster MB, 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(4):299-310.
38. Kato N, Kitaura J, Doki N, et al. Two types of C/EBPa mutations play distinct but collaborative roles in leukemogenesis: lessons from clinical data and BMT models. Blood. 2011;117(1): 221-233.
39. Paschka P, Marcucci G, Ruppert AS, et al; Cancer and Leukemia Group B. Adverse prognostic significance of KIT mutations in adult acute myeloid leukemia with inv(16) and t(8;21): a Cancer and Leukemia Group B Study. J Clin Oncol. 2006;24(24):3904-3911.
40. Gilliland DG, Griffin JD. Role of FLT3 in leukemia. Curr Opin Hematol. 2002;9(4):274-281.
41. Callens C, Chevret S, Cayuela JM, et al; European APL Group. Prognostic implication of FLT3 and Ras gene mutations in patients with acute promyelocytic leukemia (APL): a retrospective study from the European APL Group. Leukemia. 2005;19(7):1153-1160.
42. Corm S, Biggio V, Roche-Lestienne C, et al. Coexistence of AML1/RUNX1 and BCR-ABL point mutations in an imatinib-resistant form of CML. Leukemia. 2005;19(11):1991-1992.
43. Schessl C, Rawat VP, Cusan M, et al. The AML1-ETO fusion gene and the FLT3 length mutation collaborate in inducing acute leukemia in mice. J Clin Invest. 2005;115(8):2159-2168.
44. Kim HG, Kojima K, Swindle CS, et al. FLT3-ITD cooperates with inv(16) to promote progression to acute myeloid leukemia. Blood. 2008;111(3): 1567-1574.
45. Cuenco GM, Ren R. Cooperation of BCR-ABL and AML1/MDS1/EVI1 in blocking myeloid differentiation and rapid induction of an acute myelogenous leukemia. Oncogene. 2001;20(57): 8236-8248.
46. Vegesna V, Takeuchi S, Hofmann WK, et al. C/EBP-beta, C/EBP-delta, PU.1, AML1 genes: mutational analysis in 381 samples of hematopoietic and solid malignancies. Leuk Res. 2002;26(5):451-457.
47. Wethmar K, Smink JJ, Leutz A. Upstream open reading frames: molecular switches in (patho) physiology. Bioessays. 2010;32(10):885-893.
48. Sauvageau M, Miller M, Lemieux S, Lessard J, Hebert J, Sauvageau G. Quantitative expression profiling guided by common retroviral insertion sites reveals novel and cell type specific cancer genes in leukemia. Blood. 2008;111(2):790-799.
49. Theodorou V, Kimm MA, Boer M, et al. MMTV insertional mutagenesis identifies genes, gene families and pathways involved in mammary cancer. Nat Genet. 2007;39(6):759-769.
50. Mochizuki N, Shimizu S, Nagasawa T, et al. A novel gene, MEL1, mapped to 1p36.3 is highly homologous to the MDS1/EVI1 gene and is transcriptionally activated in t(1;3)(p36;q21)-positive leukemia cells. Blood. 2000;96(9): 3209-3214.
51. Aguilo F, Avagyan S, Labar A, et al. Prdm16 is a physiologic regulator of hematopoietic stem cells. Blood. 2011;117(19):5057-5066.