Essential role of PU.1 in maintenance of mixed lineage leukemia-associated leukemic stem cells

Cancer Science

Volumn 106, Issue 3, 2015, Pages 227-236

  Aikawa, Yukiko ^a   Yamagata, Kazutsune ^a   Katsumoto, Takuo ^a   Shima, Yutaka ^a   Shino, Mika ^a   Stanley, E Richard ^b   Cleary, Michael L ^c   Akashi, Koichi ^d   Tenen, Daniel G ^e,f   Kitabayashi, Issay ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d KYUSHU UNIVERSITY   (Japan)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Acute myeloid leukemia; CSF 1R; Mixed lineage leukemia; Spi 1; Stem cells

Indexed keywords

AP 20187; CYTARABINE; KI 20227; MIXED LINEAGE LEUKEMIA PROTEIN; PHOSPHOTRANSFERASE INHIBITOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CSF 1R; TRANSCRIPTION FACTOR PU 1; UNCLASSIFIED DRUG; AP20187; CARBANILAMIDE DERIVATIVE; COLONY STIMULATING FACTOR RECEPTOR; HISTONE LYSINE METHYLTRANSFERASE; HYBRID PROTEIN; MLL PROTEIN, MOUSE; N-(4-((6,7-DIMETHOXY-4-QUINOLYL)OXY)-2-METHOXYPHENYL)-N'-(1-(1,3-THIAZOLE-2-YL)ETHYL)UREA; ONCOPROTEIN; PROTO-ONCOGENE PROTEIN SPI-1; TACROLIMUS; THIAZOLE DERIVATIVE; TRANSACTIVATOR PROTEIN;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER SURVIVAL; CELL IMMORTALIZATION; DRUG TARGETING; GENE DELETION; GENE EXPRESSION; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; LEUKEMOGENESIS; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN INTERACTION; RECEPTOR UPREGULATION; SURVIVAL TIME; ACUTE MYELOBLASTIC LEUKEMIA; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CANCER STEM CELL; CARCINOGENESIS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HOMEOBOX; MORTALITY; PROGNOSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; CARCINOGENESIS; GENE EXPRESSION REGULATION, LEUKEMIC; GENES, HOMEOBOX; HISTONE-LYSINE N-METHYLTRANSFERASE; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NEOPLASTIC STEM CELLS; PHENYLUREA COMPOUNDS; PROGNOSIS; PROTO-ONCOGENE PROTEINS; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TACROLIMUS; THIAZOLES; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84925792081     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.12593     Document Type: Article

References (40)

1. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730-7.
2. Warner JK, Wang JC, Hope KJ, Jin L, Dick JE. Concepts of human leukemic development. Oncogene 2004; 23: 7164-77.
3. Ayton PM, Cleary ML. Molecular mechanisms of leukemogenesis mediated by MLL fusion proteins. Oncogene 2001; 20: 5695-707.
4. Krivtsov AV, Armstrong SA. MLL translocations, histone modifications and leukaemia stem-cell development. Nat Rev Cancer 2007; 7: 823-33.
5. Dou Y, Hess JL. Mechanisms of transcriptional regulation by MLL and its disruption in acute leukemia. Int J Hematol 2008; 87: 10-8.
6. Rodriguez-Perales S, Cano F, Lobato MN, Rabbitts TH. MLL gene fusions in human leukaemias: in vivo modelling to recapitulate these primary tumourigenic events. Int J Hematol 2008; 87: 3-9.
7. Cozzio A, Passegue E, Ayton PM, Karsunky H, Cleary ML, Weissman IL. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev 2003; 17: 3029-35.
8. Huntly BJ, 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: 587-96.
9. Armstrong SA, Staunton JE, Silverman LB et al. MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat Genet 2002; 30: 41-7.
10. Rozovskaia T, Feinstein E, Mor O et al. Upregulation of Meis1 and HoxA9 in acute lymphocytic leukemias with the t(4: 11) abnormality. Oncogene 2001; 20: 874-8.
11. Yeoh EJ, Ross ME, Shurtleff SA et al. Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell 2002; 1: 133-43.
12. Ayton PM, Cleary ML. Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev 2003; 17: 2298-307.
13. Kumar AR, Hudson WA, Chen W, Nishiuchi R, Yao Q, Kersey JH. Hoxa9 influences the phenotype but not the incidence of Mll-AF9 fusion gene leukemia. Blood 2004; 103: 1823-8.
14. Wong P, Iwasaki M, Somervaille TC, So CW, Cleary ML. Meis1 is an essential and rate-limiting regulator of MLL leukemia stem cell potential. Genes Dev 2007; 21: 2762-74.
15. Kumar AR, Li Q, Hudson WA et al. A role for MEIS1 in MLL-fusion gene leukemia. Blood 2009; 113: 1756-8.
16. Somervaille TC, Cleary ML. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell 2006; 10: 257-68.
17. Burnett SH, Kershen EJ, Zhang J et al. Conditional macrophage ablation in transgenic mice expressing a Fas-based suicide gene. J Leukoc Biol 2004; 75: 612-23.
18. Dai XM, Ryan GR, Hapel AJ et al. Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 2002; 99: 111-20.
19. Iwasaki H, Somoza C, Shigematsu H et al. Distinctive and indispensable roles of PU.1 in maintenance of hematopoietic stem cells and their differentiation. Blood 2005; 106: 1590-600.
20. Seibler J, Zevnik B, Kuter-Luks B et al. Rapid generation of inducible mouse mutants. Nucleic Acids Res 2003; 31: e12.
21. Morita S, Kojima T, Kitamura T. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther 2000; 7: 1063-6.
22. Ohno H, Kubo K, Murooka H et al. A c-fms tyrosine kinase inhibitor, Ki20227, suppresses osteoclast differentiation and osteolytic bone destruction in a bone metastasis model. Mol Cancer Ther 2006; 5: 2634-43.
23. Zhang DE, Hetherington CJ, Chen HM, Tenen DG. The macrophage transcription factor PU.1 directs tissue-specific expression of the macrophage colony-stimulating factor receptor. Mol Cell Biol 1994; 14: 373-81.
24. Yokoyama A, Kitabayashi I, Ayton PM, Cleary ML, Ohki M. Leukemia proto-oncoprotein MLL is proteolytically processed into 2 fragments with opposite transcriptional properties. Blood 2002; 100: 3710-8.
25. Aikawa Y, Katsumoto T, Zhang P et al. PU.1-mediated upregulation of CSF1R is crucial for leukemia stem cell potential induced by MOZ-TIF2. Nat Med 2010; 16: 580-5, 1p following 5.
26. Kikushige Y, Shima T, Takayanagi S et al. TIM-3 is a promising target to selectively kill acute myeloid leukemia stem cells. Cell Stem Cell 2010; 7: 708-17.
27. DiMartino JF, Ayton PM, Chen EH, Naftzger CC, Young BD, Cleary ML. The AF10 leucine zipper is required for leukemic transformation of myeloid progenitors by MLL-AF10. Blood 2002; 99: 3780-5.
28. Zhang DE, Hetherington CJ, Meyers S et al. CCAAT enhancer-binding protein (C/EBP) and AML1 (CBF alpha2) synergistically activate the macrophage colony-stimulating factor receptor promoter. Mol Cell Biol 1996; 16: 1231-40.
29. Huang G, Zhao X, Wang L et al. The ability of MLL to bind RUNX1 and methylate H3K4 at PU.1 regulatory regions is impaired by MDS/AML-associated RUNX1/AML1 mutations. Blood 2011; 118: 6544-52.
30. Yokoyama A, Cleary ML. Menin critically links MLL proteins with LEDGF on cancer-associated target genes. Cancer Cell 2008; 14: 36-46.
31. Milne TA, Briggs SD, Brock HW et al. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol Cell 2002; 10: 1107-17.
32. Walsh JC, DeKoter RP, Lee HJ et al. Cooperative and antagonistic interplay between PU.1 and GATA-2 in the specification of myeloid cell fates. Immunity 2002; 17: 665-76.
33. Gisselbrecht S, Fichelson S, Sola B et al. Frequent c-fms activation by proviral insertion in mouse myeloblastic leukaemias. Nature 1987; 329: 259-61.
34. Chitu V, Stanley ER. Colony-stimulating factor-1 in immunity and inflammation. Curr Opin Immunol 2006; 18: 39-48.
35. Huynh D, Dai XM, Nandi S et al. Colony stimulating factor-1 dependence of paneth cell development in the mouse small intestine. Gastroenterology 2009; 137: 136-44, 44 e1-3.
36. Pixley FJ, Stanley ER. CSF-1 regulation of the wandering macrophage: complexity in action. Trends Cell Biol 2004; 14: 628-38.
37. Krivtsov AV, Twomey D, Feng Z et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 2006; 442: 818-22.
38. Yokoyama A, Wang Z, Wysocka J et al. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol Cell Biol 2004; 24: 5639-49.
39. Gilliland DG, Griffin JD. The roles of FLT3 in hematopoiesis and leukemia. Blood 2002; 100: 1532-42.
40. Lavau C, Szilvassy SJ, Slany R, Cleary ML. Immortalization and leukemic transformation of a myelomonocytic precursor by retrovirally transduced HRX-ENL. EMBO J 1997; 16: 4226-37.