Retroviral insertional mutagenesis identifies genes that collaborate with NUP98-HOXD13 during leukemic transformation

Cancer Research

Volumn 67, Issue 11, 2007, Pages 5148-5155

  Slape, Christopher ^a   Hartung, Helge ^a   Lin, Ying Wei ^a   Bies, Juraj ^b   Wolff, Linda ^b   Aplan, Peter D ^a,c,d  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b NATIONAL CANCER INSTITUTE   (United States)

^c TENRI HOSPITAL   (Japan)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOPORIN 98;

ACUTE LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GENE FUSION; GENE IDENTIFICATION; GENE INSERTION; GENE LOCUS; GENETIC TRANSFORMATION; LEUKEMOGENESIS; MOUSE; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RETROVIRUS; TRANSGENE; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CLONING, MOLECULAR; ETHER-A-GO-GO POTASSIUM CHANNELS; GATA2 TRANSCRIPTION FACTOR; HOMEODOMAIN PROTEINS; LEUKEMIA, LYMPHOCYTIC, ACUTE; LEUKEMIA, MYELOID; MICE; MICE, TRANSGENIC; MICRORNAS; MOLONEY MURINE LEUKEMIA VIRUS; MUTAGENESIS, INSERTIONAL; NEOPLASM PROTEINS; NIH 3T3 CELLS; NUCLEAR PORE COMPLEX PROTEINS; ONCOGENE PROTEINS; ONCOGENE PROTEINS, FUSION; TRANSCRIPTION FACTORS;

EID: 34347213447     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-0075     Document Type: Article

References (49)

1. Raza-Egilmez SZ, Jani-Sait SN, Grossi M, Higgins MJ, Shows TB, Aplan PD. NUP98-13 gene fusion in therapy-related acute myelogenous leukemia. Cancer Res 1998;58:4269-73.
2. Lin YW, Slape C, Zhang Z, Aplan PD. NUP98-13 transgenic mice develop a highly penetrant, severe myelodysplastic syndrome that progresses to acute leukemia. Blood 2005;106:287-95.
3. Gilliland DG, Tallman MS. Focus on acute leukemias. Cancer Cell 2002;1:417-20.
4. + hematopoietic cells. Cancer Res 2006;66:6628-37.
5. Pineault N, Abramovich C, Humphries RK. Transplantable cell lines generated with NUP98-Hox fusion genes undergo leukemic progression by Meis1 independent of its binding to DNA. Leukemia 2005;19:636-43.
6. Mitchell RS, Beitzel BF, Schroder AR, et al. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2004;2:E234.
7. Bushman FD. Targeting survival: integration site selection by retroviruses and LTR-retrotransposons. Cell 2003;115:135-8.
8. Wu X, Li Y, Crise B, Burgess SM. Transcription start regions in the human genome are favored targets for MLV integration. Science 2003;300:1749-51.
9. Uren AG, Kool J, Berns A, van Lohuizen M. Retroviral insertional mutagenesis: past, present and future. Oncogene 2005;24:7656-72.
10. Li J, Shen H, Himmel KL, et al. Leukemia disease genes: large-scale cloning and pathway predictions. Nat Genet 1999;23:348-53.
11. Lund AH, Turner G, Trubetskoy A, et al. Genome-wide retroviral insertional tagging of genes involved in cancer in Cdkn2a-deficient mice. Nat Genet 2002;32:160-5.
12. Castilla LH, Perrat P, Martinez NJ, et al. Identification of genes that synergize with Cbfb-MYH11 in the pathogenesis of acute myeloid leukemia. Proc Natl Acad Sci U S A 2004;101:4924-9.
13. Wolff L. Retroviral insertional mutagenesis and its application to genetically engineered mice. In: Thebault S, editor. Progress in virus research. Hauppauge (NY): Nova Science Publishers; 2006. p. 267-99.
14. Lin YW, Nichols RA, Letterio JJ, Aplan PD. Notch1 mutations are important for leukemic transformation in murine models of precursor-T leukemia/lymphoma. Blood 2006;107:2540-3.
15. Wolff L, Koller R, Hu X, Anver MR. A Moloney murine leukemia virus-based retrovirus with 4070A long terminal repeat sequences induces a high incidence of myeloid as well as lymphoid neoplasms. J Virol 2003;77:4965-71.
16. Rowe WP, Pugh WE, Hartley JW. Plaque assay techniques for murine leukemia viruses. Virology 1970;42:1136-9.
17. Kogan SC, Ward JM, Anver MR, et al. Bethesda proposals for classification of nonlymphoid hematopoietic neoplasms in mice. Blood 2002;100:238-45.
18. Morse HC III, Anver MR, Fredrickson TN, et al. Bethesda proposals for classification of lymphoid neoplasms in mice. Blood 2002;100:246-58.
19. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) Method. Methods 2001;25:402-8.
20. Hwang HC, Martins CP, Bronkhorst Y, et al. Identification of oncogenes collaborating with p27Kip1 loss by insertional mutagenesis and high-throughput insertion site analysis. Proc Natl Acad Sci U S A 2002;99:11293-8.
21. Pineault N, Buske C, Feuring-Buske M, et al. Induction of acute myeloid leukemia in mice by the human leukemia-specific fusion gene NUP98-13 in concert with Meis1. Blood 2003;101:4529-38.
22. Iwasaki M, Kuwata T, Yamazaki Y, et al. Identification of cooperative genes for NUP98-9 in myeloid leukemo-genesis using a mouse model. Blood 2005;105:784-93.
23. Ghinassi B, Sanchez M, Martelli F, et al. The hypomorphic Gata1low mutation alters the proliferation/differentiation potential of the common megakaryocytic-erythroid progenitor. Blood 2007;109:1460-71.
24. Migliaccio AR, Rana RA, Sanchez M, et al. GATA-1 as a regulator of mast cell differentiation revealed by the phenotype of the GATA-1low mouse mutant. J Exp Med 2003;197:281-96.
25. Martin DI, Zon LI, Mutter G, Orkin SH. Expression of an erythroid transcription factor in megakaryocytic and mast cell lineages. Nature 1990;344:444-7.
26. Akagi K, Suzuki T, Stephens RM, Jenkins NA, Copeland NG. RTCGD: retroviral tagged cancer gene database. Nucleic Acids Res 2004;32:D523-7.
27. Kelly LM, Gilliland DG. Genetics of myeloid leukemias. Annu Rev Genomics Hum Genet 2002;3:179-98.
28. Moskow JJ, Bullrich F, Huebner K, Daar IO, Buchberg AM. Meis1, a PBX1-related homeobox gene involved in myeloid leukemia in BXH-2 mice. Mol Cell Biol 1995;15:5434-43.
29. Nakamura T, Largaespada DA, Lee MP, et al. Fusion of the nucleoporin gene NUP98 to HOXA9 by the chromosome translocation t(7;11)(p15;p15) in human myeloid leukaemia. Nat Genet 1996;12:154-8.
30. Kroon E, Krosl J, Thorsteinsdottir U, Baban S, Buchberg AM, Sauvageau G. Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. EMBO J 1998;17:3714-25.
31. Thorsteinsdottir U, Kroon E, Jerome L, Blasi F, Sauvageau G. Defining roles for HOX and MEIS1 genes in induction of acute myeloid leukemia. Mol Cell Biol 2001;21:224-34.
32. Kroon E, Thorsteinsdottir U, Mayotte N, Nakamura T, Sauvageau G. NUP98-9 expression in hemopoietic stem cells induces chronic and acute myeloid leukemias in mice. EMBO J 2001;20:350-61.
33. van Wely KH, Molijn AC, Buijs A, et al. The MN1 oncoprotein synergizes with coactivators RAC3 and p300 in RAR-RXR-mediated transcription. Oncogene 2003;22:699-709.
34. Buijs A, Sherr S, van Baal S, et al. Translocation (12;22) (p13;q11) in myeloproliferative disorders results in fusion of the ETS-like TEL gene on 12p13 to the MN1 gene on 22q11. Oncogene 1995;10:1511-9.
35. Heuser M, Beutel G, Krauter J, et al. High meningioma 1 (MN1) expression as a predictor for poor outcome in acute myeloid leukemia with normal cytogenetics. Blood 2006;108:3898-905.
36. Kawagoe H, Grosveld GC. Conditional MN1-TEL knock-in mice develop acute myeloid leukemia in conjunction with overexpression of HOXA9. Blood 2005;106:4269-77.
37. Roth MJ, Tanese N, Goff SP. Gene product of Moloney murine leukemia virus required for proviral integration is a DNA-binding protein. J Mol Biol 1988;203:131-9.
38. Wieser R, Volz A, Vinatzer U, et al. Transcription factor GATA-2 gene is located near 3q21 breakpoints in myeloid leukemia. Biochem Biophys Res Commun 2000;273:239-45.
39. Ohyashiki JH, Ohyashiki K, Shimamoto T, et al. Ecotropic virus integration site-1 gene preferentially expressed in post-myelodysplasia acute myeloid leukemia: possible association with GATA-1, GATA-2, and stem cell leukemia gene expression. Blood 1995;85:3713-8.
40. Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 2006;103:2257-61.
41. He H, Jazdzewski K, Li W, et al. The role of microRNA genes in papillary thyroid carcinoma. Proc Natl Acad Sci U S A 2005;102:19075-80.
42. Yu J, Wang F, Yang GH, et al. Human microRNA clusters: genomic organization and expression profile in leukemia cell lines. Biochem Biophys Res Commun 2006;349:59-68.
43. Johansson FK, Brodd J, Eklof C, et al. Identification of candidate cancer-causing genes in mouse brain tumors by retroviral tagging. Proc Natl Acad Sci U S A 2004;101:11334-7.
44. Si ML, Zhu S, Wu H, Lu Z, Wu F, Mo YY. miR-21-mediated tumor growth. Oncogene 2006 Oct 30 [Epub ahead of print].
45. Chan JA, Krichevsky AM, Kosik KS. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 2005;65:6029-33.
46. Iorio MV, Ferracin M, Liu CG, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res 2005;65:7065-70.
47. Hess JL. MLL: a histone methyltransferase disrupted in leukemia. Trends Mol Med 2004;10:500-7.
48. Golub TR, Slonim DK, Tamayo P, et al. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 1999;286:531-7.
49. Marcucci G, Baldus CD, Ruppert AS, et al. Overexpression of the ETS-related gene, ERG, predicts a worse outcome in acute myeloid leukemia with normal karyotype: a Cancer and Leukemia Group B study. J Clin Oncol 2005;23:9234-42.