Mir-10a overexpression is associated with npm1 mutations and mdm4 downregulation in intermediate-risk acute myeloid leukemia

Experimental Hematology

Volumn 39, Issue 10, 2011, Pages

  Ovcharenko, Dmitriy ^a,b   Stölzel, Friedrich ^c   Poitz, David ^c   Fierro, Fernando ^c   Schaich, Markus ^c   Neubauer, Andreas ^d   Kelnar, Kevin ^a   Davison, Timothy ^a   Müller Tidow, Carsten ^e   Thiede, Christian ^c   Bornhäuser, Martin ^c   Ehninger, Gerhard ^c   Brown, David ^a   Illmer, Thomas ^c  

^a ASURAGEN INC   (United States)

^b Altogen Labs   (United States)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d UNIVERSITY HOSPITAL MARBURG   (Germany)

^e UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; LUCIFERASE; MICRORNA; MICRORNA 10A; PROTEIN MDMX; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ADULT; ARTICLE; BONE MARROW; CANCER RISK; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; ENZYME ASSAY; FEMALE; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE MUTATION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC RISK; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LEUKEMIA CELL; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; MURINE DOUBLE MINUTE 4 GENE; NUCLEOPHOSMIN 1 GENE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; UPREGULATION; VALIDATION STUDY; WESTERN BLOTTING; WILD TYPE;

MURINAE;

EID: 80052855368     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2011.07.008     Document Type: Article

References (71)

1. Lowenberg B. Acute myeloid leukemia: the challenge of capturing disease variety. Hematology Am Soc Hematol Educ Program 2008, 1-11.
2. Bloomfield C.D., Shuma C., Regal L., et al. Long-term survival of patients with acute myeloid leukemia: a third follow-up of the Fourth International Workshop on Chromosomes in Leukemia. Cancer 1997, 80:2191-2198.
3. Mrozek K., Marcucci G., Paschka P., Whitman S.P., Bloomfield C.D. Clinical relevance of mutations and gene-expression changes in adult acute myeloid leukemia with normal cytogenetics: are we ready for a prognostically prioritized molecular classification?. Blood 2007, 109:431-448.
4. Kiyoi H., Naoe T., Nakano Y., et al. Prognostic implication of FLT3 and N-RAS gene mutations in acute myeloid leukemia. Blood 1999, 93:3074-3080.
5. Pabst T., Mueller B.U., Zhang P., et al. Dominant-negative mutations of CEBPA, encoding CCAAT/enhancer binding protein-alpha (C/EBPalpha), in acute myeloid leukemia. Nat Genet 2001, 27:263-270.
6. Falini B., Mecucci C., Tiacci E., et al. Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N Engl J Med 2005, 352:254-266.
7. Frohling S., Schlenk R.F., Breitruck J., et al. Prognostic significance of activating FLT3 mutations in younger adults (16 to 60 years) with acute myeloid leukemia and normal cytogenetics: a study of the AML Study Group Ulm. Blood 2002, 100:4372-4380.
8. Kottaridis P.D., Gale R.E., Frew M.E., et al. The presence of a FLT3 internal tandem duplication in patients with acute myeloid leukemia (AML) adds important prognostic information to cytogenetic risk group and response to the first cycle of chemotherapy: analysis of 854 patients from the United Kingdom Medical Research Council AML 10 and 12 trials. Blood 2001, 98:1752-1759.
9. Thiede C., Steudel C., Mohr B., et al. Analysis of FLT3-activating mutations in 979 patients with acute myelogenous leukemia: association with FAB subtypes and identification of subgroups with poor prognosis. Blood 2002, 99:4326-4335.
10. Dohner K., Schlenk R.F., Habdank M., et al. Mutant nucleophosmin (NPM1) predicts favorable prognosis in younger adults with acute myeloid leukemia and normal cytogenetics: interaction with other gene mutations. Blood 2005, 106:3740-3746.
11. Schnittger S., Schoch C., Kern W., et al. Nucleophosmin gene mutations are predictors of favorable prognosis in acute myelogenous leukemia with a normal karyotype. Blood 2005, 106:3733-3739.
12. Thiede C., Koch S., Creutzig E., et al. Prevalence and prognostic impact of NPM1 mutations in 1485 adult patients with acute myeloid leukemia (AML). Blood 2006, 107:4011-4020.
13. Brandts C.H., Sargin B., Rode M., et al. Constitutive activation of Akt by Flt3 internal tandem duplications is necessary for increased survival, proliferation, and myeloid transformation. Cancer Res 2005, 65:9643-9650.
14. Levis M., Pham R., Smith B.D., Small D. In vitro studies of a FLT3 inhibitor combined with chemotherapy: sequence of administration is important to achieve synergistic cytotoxic effects. Blood 2004, 104:1145-1150.
15. Cheng K., Grisendi S., Clohessy J.G., et al. The leukemia-associated cytoplasmic nucleophosmin mutant is an oncogene with paradoxical functions: Arf inactivation and induction of cellular senescence. Oncogene 2007, 26:7391-7400.
16. Colombo E., Bonetti P., Lazzerini Denchi E., et al. Nucleophosmin is required for DNA integrity and p19Arf protein stability. Mol Cell Biol 2005, 25:8874-8886.
17. Alcalay M., Tiacci E., Bergomas R., et al. Acute myeloid leukemia bearing cytoplasmic nucleophosmin (NPMc+ AML) shows a distinct gene expression profile characterized by up-regulation of genes involved in stem-cell maintenance. Blood 2005, 106:899-902.
18. Mullighan C.G., Kennedy A., Zhou X., et al. Pediatric acute myeloid leukemia with NPM1 mutations is characterized by a gene expression profile with dysregulated HOX gene expression distinct from MLL-rearranged leukemias. Leukemia 2007, 21:2000-2009.
19. Bullinger L., Dohner K., Bair E., et al. Use of gene-expression profiling to identify prognostic subclasses in adult acute myeloid leukemia. N Engl J Med 2004, 350:1605-1616.
20. Radmacher M.D., Marcucci G., Ruppert A.S., et al. Independent confirmation of a prognostic gene-expression signature in adult acute myeloid leukemia with a normal karyotype: a Cancer and Leukemia Group B study. Blood 2006, 108:1677-1683.
21. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
22. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
23. Eulalio A., Huntzinger E., Izaurralde E. Getting to the root of miRNA-mediated gene silencing. Cell 2008, 132:9-14.
24. Hornstein E., Mansfield J.H., Yekta S., et al. The microRNA miR-196 acts upstream of Hoxb8 and Shh in limb development. Nature 2005, 438:671-674.
25. Hornstein E., Shomron N. Canalization of development by microRNAs. Nat Genet 2006, 38(suppl):S20-S24.
26. Chen C.Z., Li L., Lodish H.F., Bartel D.P. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004, 303:83-86.
27. 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.
28. Fukao T., Fukuda Y., Kiga K., et al. An evolutionarily conserved mechanism for microRNA-223 expression revealed by microRNA gene profiling. Cell 2007, 129:617-631.
29. Garzon R., Pichiorri F., Palumbo T., et al. MicroRNA gene expression during retinoic acid-induced differentiation of human acute promyelocytic leukemia. Oncogene 2007, 26:4148-4157.
30. Lu J., Getz G., Miska E.A., et al. MicroRNA expression profiles classify human cancers. Nature 2005, 435:834-838.
31. Mi S., Lu J., Sun M., et al. MicroRNA expression signatures accurately discriminate acute lymphoblastic leukemia from acute myeloid leukemia. Proc Natl Acad Sci U S A 2007, 104:19971-19976.
32. Calin G.A., Croce C.M. Chromosomal rearrangements and microRNAs: a new cancer link with clinical implications. J Clin Invest 2007, 117:2059-2066.
33. Fazi F., Racanicchi S., Zardo G., et al. Epigenetic silencing of the myelopoiesis regulator microRNA-223 by the AML1/ETO oncoprotein. Cancer Cell 2007, 12:457-466.
34. Garzon R., Volinia S., Liu C.G., et al. MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. Blood 2008, 111:3183-3189.
35. Schaich M., Koch R., Soucek S., Repp R., Ehninger G., Illmer T. A sensitive model for prediction of relapse in adult acute myeloid leukaemia with t(8;21) using white blood cell count, CD56 and MDR1 gene expression at diagnosis. Br J Haematol 2004, 125:477-479.
36. Schaich M., Ritter M., Illmer T., et al. Mutations in ras proto-oncogenes are associated with lower mdr1 gene expression in adult acute myeloid leukaemia. Br J Haematol 2001, 112:300-307.
37. Quentmeier H., Martelli M.P., Dirks W.G., et al. Cell line OCI/AML3 bears exon-12 NPM gene mutation-A and cytoplasmic expression of nucleophosmin. Leukemia 2005, 19:1760-1767.
38. Shingara J., Keiger K., Shelton J., et al. An optimized isolation and labeling platform for accurate microRNA expression profiling. RNA 2005, 11:1461-1470.
39. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
40. Stolzel F., Steudel C., Oelschlagel U., et al. Mechanisms of resistance against PKC412 in resistant FLT3-ITD positive human acute myeloid leukemia cells. Ann Hematol 2010.
41. Illmer T., Schaich M., Platzbecker U., et al. P-glycoprotein-mediated drug efflux is a resistance mechanism of chronic myelogenous leukemia cells to treatment with imatinib mesylate. Leukemia 2004, 18:401-408.
42. Killion P.J., Sherlock G., Iyer V.R. The Longhorn Array Database (LAD): an open-source, MIAME compliant implementation of the Stanford Microarray Database (SMD). BMC Bioinformatics 2003, 4:32.
43. Hochberg Y., Benjamini Y. More powerful procedures for multiple significance testing. Stat Med 1990, 9:811-818.
44. Vaquerizas J.M., Conde L., Yankilevich P., et al. GEPAS, an experiment-oriented pipeline for the analysis of microarray gene expression data. Nucleic Acids Res. 2005, 33:W616-W620.
45. Isken F., Steffen B., Merk S., et al. Identification of acute myeloid leukaemia associated microRNA expression patterns. Br J Haematol 2008, 140:153-161.
46. Falini B., Nicoletti I., Martelli M.F., Mecucci C. Acute myeloid leukemia carrying cytoplasmic/mutated nucleophosmin (NPMc+ AML): biologic and clinical features. Blood 2007, 109:874-885.
47. Garzon R., Garofalo M., Martelli M.P., et al. Distinctive microRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin. Proc Natl Acad Sci U S A 2008, 105:3945-3950.
48. Garzon R., Pichiorri F., Palumbo T., et al. MicroRNA fingerprints during human megakaryocytopoiesis. Proc Natl Acad Sci U S A 2006, 103:5078-5083.
49. Ma L., Teruya-Feldstein J., Weinberg R.A. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007, 449:682-688.
50. Mansfield J.H., Harfe B.D., Nissen R., et al. MicroRNA-responsive 'sensor' transgenes uncover Hox-like and other developmentally regulated patterns of vertebrate microRNA expression. Nat Genet 2004, 36:1079-1083.
51. Colombo E., Marine J.C., Danovi D., Falini B., Pelicci P.G. Nucleophosmin regulates the stability and transcriptional activity of p53. Nat Cell Biol 2002, 4:529-533.
52. Altucci L., Gronemeyer H. The promise of retinoids to fight against cancer. Nat Rev Cancer 2001, 1:181-193.
53. Wiley S.R., Schooley K., Smolak P.J., et al. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 1995, 3:673-682.
54. Kruse J.P., Gu W. Modes of p53 regulation. Cell 2009, 137:609-622.
55. Marine J.C., Francoz S., Maetens M., Wahl G., Toledo F., Lozano G. Keeping p53 in check: essential and synergistic functions of Mdm2 and Mdm4. Cell Death Differ 2006, 13:927-934.
56. den Besten W., Kuo M.L., Williams R.T., Sherr C.J. Myeloid leukemia-associated nucleophosmin mutants perturb p53-dependent and independent activities of the Arf tumor suppressor protein. Cell Cycle 2005, 4:1593-1598.
57. Harutyunyan A., Klampfl T., Cazzola M., Kralovics R. p53 lesions in leukemic transformation. N Engl J Med 2011, 364:488-490.
58. Francoz S., Froment P., Bogaerts S., et al. Mdm4 and Mdm2 cooperate to inhibit p53 activity in proliferating and quiescent cells in vivo. Proc Natl Acad Sci U S A 2006, 103:3232-3237.
59. Long J., Parkin B., Ouillette P., et al. Multiple distinct molecular mechanisms influence sensitivity and resistance to MDM2 inhibitors in adult acute myelogenous leukemia. Blood 2010, 116:71-80.
60. Mishra P.J., Humeniuk R., Longo-Sorbello G.S., Banerjee D., Bertino J.R. A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance. Proc Natl Acad Sci U S A 2007, 104:13513-13518.
61. Wang Q., Huang Z., Xue H., et al. MicroRNA miR-24 inhibits erythropoiesis by targeting activin type I receptor ALK4. Blood 2008, 111:588-595.
62. Felli N., Fontana L., Pelosi E., et al. MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythroleukemic cell growth via kit receptor down-modulation. Proc Natl Acad Sci U S A 2005, 102:18081-18086.
63. le Sage C., Nagel R., Egan D.A., et al. Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J 2007, 26:3699-3708.
64. Christoffersen N.R., Silahtaroglu A., Orom U.A., Kauppinen S., Lund A.H. miR-200b mediates post-transcriptional repression of ZFHX1B. RNA 2007, 13:1172-1178.
65. Liu H., Brannon A.R., Reddy A.R., et al. Identifying mRNA targets of microRNA dysregulated in cancer: with application to clear cell Renal Cell Carcinoma. BMC Syst Biol 2010, 4:51.
66. Cimmino A., Calin G.A., Fabbri M., et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci U S A 2005, 102:13944-13949.
67. Kulshreshtha R., Ferracin M., Wojcik S.E., et al. A microRNA signature of hypoxia. Mol Cell Biol 2007, 27:1859-1867.
68. Kimura H., Kawasaki H., Taira K. Mouse microRNA-23b regulates expression of Hes1 gene in P19 cells. Nucleic Acids Symp Ser (Oxf) 2004, 213-214.
69. He L., Thomson J.M., Hemann M.T., et al. A microRNA polycistron as a potential human oncogene. Nature 2005, 435:828-833.
70. O'Donnell K.A., Wentzel E.A., Zeller K.I., Dang C.V., Mendell J.T. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005, 435:839-843.
71. Jiang Y., Wu Y., Greenlee A.R., et al. miR-106a-mediated malignant transformation of cells induced by anti-benzo[a]pyrene-trans-7,8-diol-9,10-epoxide. Toxicol Sci 2011, 119:50-60.