Sfpi1/PU.1 mutations in mouse radiation-induced acute myeloid leukaemias affect mRNA and protein abundance and associate with disrupted transcription

Leukemia Research

Volumn 35, Issue 1, 2011, Pages 126-132

  Brown, N L ^a   Finnon, R ^a   Bulman, R A ^a   Finnon, P ^a   Moody, J ^a   Bouffler, S D ^a   Badie, C ^a  

^a PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

Mutation; Myeloid leukaemia; Phosphorylation; Radiation; Sfpi1 PU.1; Transcription

Indexed keywords

CD135 ANTIGEN; MESSENGER RNA; PROTEIN SFPI1; TRANSCRIPTION FACTOR PU 1; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE DOSAGE; GENE EXPRESSION; LEUKEMIA CELL LINE; LEUKEMOGENESIS; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN FUNCTION; RADIATION CARCINOGENESIS; TARGET CELL; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINE, TUMOR; CELL LINEAGE; CHROMOSOMES, ARTIFICIAL, BACTERIAL; GENE EXPRESSION REGULATION, NEOPLASTIC; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; LEUKEMIA, MYELOID, ACUTE; LEUKEMIA, RADIATION-INDUCED; MICE; MUTATION; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 78650172042     PISSN: 01452126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.leukres.2010.06.015     Document Type: Article

References (48)

1. Scott E.W., Simon M.C., Anastasi J., Singh H. Requirement of transcription factor PU.1 in the development of multiple haematopoietic lineages. Science 1994, 264:1573-1577.
2. McKercher S.R., Torbett B.E., Anderson K.C., Henkel G.W., Vestal D.J., Baribault H., et al. Targeted disruption of the PU.1 gene results in multiple haematopoietic abnormalities. EMBO J 1996, 15:5647-5658.
3. Mueller B.U., Pabst T., Osato M., Asou N., Johansen C.M., Minden M.D., et al. Heterozygous PU.1 mutations are associated with acute myeloid leukaemia. Blood 2002, 100:998-1007.
4. Bonadies N., Pabst T., Mueller B.U. Heterozygous deletion of the PU.1 locus in human AML. Blood 2010, 115:331-334.
5. Bonadies N., Neururer Ch, Steege A., Vallabhapurapu S., Pabst T., Mueller B.U. PU.1 is regulated by NK-kappaB through a novel binding site in a 17kb upstream enhancer element. Oncongene 2010, 29:1062-1072.
6. Vangala R.K., Heiss-Neumann M.S., Rangatia J.S., Singh S.M., Schoch C., Tenen D.G., et al. The myeloid master transcription factor PU.1 is inactivated by AML-ETO in t(8, 21) myeloid leukaemia. Blood 2003, 101:270-277.
7. Walter M.J., Park J.S., Ries R.E., Lau S.K.M., McLellan M., Jaeger S., et al. Reduced PU.1 expression causes myeloid progenitor expansion and increased leukaemia penetrance in mice expressing PML-RARalpha. Proc Natl Acad Sci USA 2005, 102:12513-12518.
8. Rosenbauer F., Wagner K., Kutok J.L., Iwasaki H., Le Beau M.M., Okuno Y., et al. Acute myeloid leukaemia induced by graded reduction of a lineage-specific transcription factor, PU. 1. Nat Genet 2004, 36:624-630.
9. Hayata I., Seki M., Yoshida K., Hirashima K., Sado T., Yamagiwa J., et al. Chromosomal aberrations observed in 52 mouse myeloid leukaemias. Cancer Res 1983, 43:367-373.
10. Trakhtenbrot L., Kranthgamer R., Resnitzky P., Haran-Ghera N. Deletion of chromosome 2 is an early event in the development of radiation-induced myeloid leukaemia in SJL/J mice. Leukaemia 1988, 2:545-550.
11. Rithidech K.N., Bond V.P., Cronkite E.P., Thompson M.H. A specific chromosomal deletion in murine leukaemic cells induced by radiation with different qualities. Exp Haematol 1993, 21:427-431.
12. Bouffler S.D., Meijn e E.I.M., Huiskamp R., Cox R. Chromosomal abnormalities in neutron-induced acute myeloid leukaemias in CBA/H mice. Radiat Res 1996, 146:349-352.
13. Silver A., Moody J., Dunford R., Clark D., Ganz S., Bulman R., et al. Molecular mapping of chromosome 2 deletions in murine radiation-induced AML localises a putative tumour suppressor gene to a 1.0 cM region homologous to human chromosome segment 11p11-12. Genes Chromosomes Cancer 1999, 24:95-104.
14. Cook W.D., McCaw B.J., Herring C., John D.L., Foote S.J., Nutt S.L., et al. PU.1 is a suppressor of myeloid leukaemia, inactivated in mice by gene deletion and mutation of its DNA binding domain. Blood 2004, 104:3437-3444.
15. Suraweera N., Meijne E., Moody J., Carvajal-Carmona L.G., Yoshida K., Pollard P., et al. Mutations of the PU.1 ETS domain are specifically associated with murine radiation-induced, but not human therapy-related, acute myeloid leukaemia. Oncogene 2005, 24:3678-3683.
16. Peng Y., Brown N., Finnon R., Warner C.L., Liu X., Genik P.C., et al. Radiation leukaemogenesis in mice: loss of PU.1 on chromosome 2 in CBA and C57BL/6 mice after irradiation with 1GeV/nucleon 56Fe ions, X rays or gamma rays. Part I. Experimental observations. Radiat Res 2009, 171:474-483.
17. Ng P.C., Henikoff S. Predicting deleterious amino acid substitutions. Genome Res 2001, 11:863-874.
18. Ramensky V., Bork P., Sunyaev S. Human non-synonymous SNPs: server and survey. Nucleic Acids Res 2002, 30:3894-3900.
19. Brunham L.R., Singaraja R.R., Pape T.D., Kejariwal A., Thomas P.D., Hayden M.R. Accurate prediction of the functional significance of single nucleotide polymorphisms and mutations in the ABCA1 gene. PLoS Genet 2005, 1:e83.
20. Capriotti E., Calabrese R., Casadio R. Predicting the insurgence of human genetic diseases associated to single point protein mutations with support vector machines and evolutionary information. Bioinformatics 2006, 22:2729-2734.
21. Bromberg Y., Rost B. SNAP: predict effect of non-synonymous polymorphisms on function. Nucleic Acids Res 2007, 11:3823-3835.
22. Miller M.L., Blom N. Kinase-specific prediction of protein phosphorylation sites. Methods Mol Biol 2009, 527:299-310.
23. Obenauer J.C., Cantley L.C., Yaffe M.B. Scansite 2.0: proteome-wide prediction of cell signalling interactions using short sequence motifs. Nucleic Acids Res 2003, 31:3635-3641.
24. Lajtha L.G. Which are the leukaemic cells?. Blood Cells 1981, 7:45-62.
25. Boggs D.R. Clonal origin of leukaemia: site of origin in the stem cell hierarchy and the significance of chromosomal changes. Blood Cells 1981, 7:205-215.
26. Gupta P., Gurudutta G.U., Verma Y.K., Kishore V., Gulati S., Sharma R.K., et al. PU.1: An ETS family transcription factor that regulates leukaemogenesis besides normal hematopoiesis. Stem Cells Dev 2006, 15:609-617.
27. Carey J.O., Posekany K.J., deVente J.E., Pettit G.R., Ways D.K. Phorbol ester-stimulated phosphorylation of PU.1: association with leukaemic cell growth inhibition. Blood 1996, 87:4316-4324.
28. Mao C., Ray-Gallet D., Tavitian A., Moreau-Gachelin F. Differential phosphorylations of Spi-B and Spi-1 transcription factors. Oncogene 1996, 12:863-873.
29. Liew C.W., Rand K.D., Simpson R.J., Yung W.W., Mansfield R.E., Crossley M., et al. Molecular analysis of the interaction between the hematopoietic master transcription factors GATA-1 and PU.1. J Biol Chem 2006, 281:28296-28306.
30. Behre G., Whitmarsh A.J., Coghlan M.P., Hoang T., Carpenter C.L., Zhang D.E., et al. c-Jun is a JNK-independent coactivator of the PU.1 transcription factor. J Biol Chem 1999, 274:4939-4946.
31. Matushansky I., Radparvar F., Skoultchi A.I. CDK6 blocks differentiation: coupling cell proliferation to the block to differentiation in leukaemic cells. Oncogene 2003, 22:4143-4149.
32. Rosnet O., Bühring H.J., Marchetto S., Rappold I., Lavagna C., Sainty D., et al. Human FLT3/FLK2 receptor tyrosine kinase is expressed at the surface of normal and malignant haematopoietic cells. Leukaemia 1996, 10:238-248.
33. Inomata M., Takahashi S., Harigae H., Kameoka J., Kaku M., Sasaki T. Inverse correlation between Flt3 and PU.1 expression in acute myeloblastic leukaemias. Leuk Res 2006, 30:659-664.
34. Carow C.E., Levenstein M., Kaufmann S.H., Chen J., Amin S., Rockwell P., et al. Expression of the hematopoietic growth factor receptor FLT3 (STK-1/Flk2) in human leukemias. Blood 1996, 87:1089-1096.
35. Akashi K., Traver D., Miyamoto T., Weissman I.L. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 2000, 404:193-197.
36. Zhang C.C., Lodish H. Murine haematopoietic stem cells change their surface phenotype during ex vivo expansion. Blood 2005, 105:4314-4320.
37. Chen H., Ray-Gallet D., Zhang P., Hetherington C.J., Gonzalez D.A., Zhang D.E., et al. PU.1 (Spi-1) autoregulates its expression in myeloid cells. Oncogene 1995, 11:1549-1560.
38. Chen H., Zhang P., Radomska H.S., Hetherinton C.J., Zhang D.-E., Tenen D.G. Octamer binding factors and their coactivator can activate the murine PU.1 (spi-1) promoter. J Biol Chem 1996, 271:15743-15752.
39. Pio F., Kodandapani R., Ni C.-Z., Shepard W., Klemsz M., McKarcher S.R., et al. New insights on DNA recognition by ets proteins from the crystal structure of the PU.1 ETS domain-DNA complex. J Biol Chem 1996, 271:23329-23337.
40. Metcalf D., Dakic A., Mifsud S., DiRago L., Wu L., Nutt S. Inactivation of PU.1 in adult mice leads to the development of myeloid leukaemia. Proc Natl Acad Sci USA 2006, 103:1486-1491.
41. Gross S.A., Zheng J.H., Le A.T., Kerzic P.J., Irons R.D. PU.1 phosphorylation correlates with hydroquinone-induced alterations in myeloid differentiation and cytokine-dependent clonogenic response in human CD34(+) haematopoietic progenitor cells. Cell Biol Toxicol 2006, 22:229-241.
42. Cuneo A., Fagioli F., Pazzi, Tallarico A., Previati R., Piva N., et al. Morphologic, immunologic and cytogenetic studies in acute myeloid leukaemia following occupational exposure to pesticides and organic solvents. Leuk Res 1992, 16:789-796.
43. Rithidech K., Dunn J.J., Bond V.P., Gordon C.R., Conkite E.P. Characterisation of genetic instability in radiation- and benzene-induced murine acute leukaemia. Mutat Res 1999, 428:33-39.
44. Choe K.S., Ujhelly O., Wontakal S.N., Skoultchi A.I. PU.1 directly regulates cdk6 expression, linking the cell proliferation and differentiation programs in erythroid cells. J Biol Chem 2010, 285:3044-3052.
45. Bouffler S.D., Meijne E.I.M., Morris D.J., Papworth D. Chromosome 2 hypersensitivity and clonal development in murine radiation acute myeloid leukaemia. Int J Radiat Biol 1997, 72:181-189.
46. Darakhshan F., Badie C., Moody J., Coster M., Finnon R., Finnon P., et al. Evidence for complex multigenic inheritance of radiation AML susceptibility in mice revealed using a surrogate phenotypic assay. Carcinogenesis 2006, 37:311-318.
47. Ban N., Kai M. Implication of replicative stress-related stem cell ageing in radiation-induced murine leukaemia. Br J Cancer 2009, 101:363-371.
48. Meshinchi S., Appelbaum F.R. Structural and functional alterations of FLT3 in acute myeloid leukaemia. Clin Cancer Res 2009, 15:4263-4269.