Best Practice & Research Clinical Haematology
Volume 22, Issue 2 , Pages 239-248 , June 2009

MicroRNA expression profiling in acute myeloid and chronic lymphocytic leukaemias

  • Guido Marcucci, MD (Professor of Medicine)

      Affiliations

    • Division of Hematology and Oncology, Department of Internal Medicine, Comprehensive Cancer Center, The Ohio State University, Columbus, OH, USA
    • Corresponding Author InformationCorresponding author. The Ohio State University, The Comprehensive Cancer Center, A433B Starling-Loving Hall, 320 West 10th Avenue, Columbus, OH 43210, USA. Tel.: +1614 293 9808; Fax: +1614 293 7527.
    • These authors contributed equally to this work.
  • ,
  • Krzysztof Mrózek, MD, PhD (Research Scientist)

      Affiliations

    • Division of Hematology and Oncology, Department of Internal Medicine, Comprehensive Cancer Center, The Ohio State University, Columbus, OH, USA
    • These authors contributed equally to this work.
  • ,
  • Michael D. Radmacher, PhD (Senior Clinical Biostatistician)

      Affiliations

    • Division of Hematology and Oncology, Department of Internal Medicine, Comprehensive Cancer Center, The Ohio State University, Columbus, OH, USA
  • ,
  • Clara D. Bloomfield, MD (Distinguished University Professor, William G. Pace III Professor of Cancer Research)

      Affiliations

    • Division of Hematology and Oncology, Department of Internal Medicine, Comprehensive Cancer Center, The Ohio State University, Columbus, OH, USA
  • ,
  • Carlo M. Croce, MD (The John W. Wolfe Chair in Human Cancer Genetics, Professor and Chairman)

      Affiliations

    • Department of Molecular Virology, Immunology and Medical Genetics, Comprehensive Cancer Center, The Ohio State University, Columbus, OH, USA

References 

  1. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–297
  2. Ambros V. The functions of animal microRNAs. Nature. 2004;431:350–355
  3. Gregory RI, Shiekhattar R. MicroRNA biogenesis and cancer. Cancer Res. 2005;65:3509–3512
  4. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006;6:857–866
  5. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215–233
  6. Calin GA, Sevignani C, Dumitru CD, et al. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci U S A. 2004;101:2999–3004
  7. Garzon R, Croce CM. MicroRNAs in normal and malignant hematopoiesis. Curr Opin Hematol. 2008;15:352–358
  8. Fabbri M, Croce CM, Calin GA. MicroRNAs in the ontogeny of leukemias and lymphomas. Leuk Lymphoma 2009;50:160–70.
  9. Chang T-C, Yu D, Lee Y-S, et al. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet. 2008;40:43–50
  10. Estey EH, Döhner H. Acute myeloid leukaemia. Lancet. 2006;368:1894–1907
  11. Estey EH. Treatment of acute myeloid leukemia. Haematologica. 2009;94:10–16
  12. Fröhling S, Döhner H. Chromosomal abnormalities in cancer. N Engl J Med. 2008;359:722–734
  13. Mrózek K, Heerema NA, Bloomfield CD. Cytogenetics in acute leukemia. Blood Rev. 2004;18:115–136
  14. Grimwade D, Walker H, Harrison G, et al. The importance of diagnostic cytogenetics on outcome in AML: analysis of 1,612 patients entered into the MRC AML 10 trial. Blood. 1998;92:2322–2333
  15. Slovak ML, Kopecky KJ, Cassileth PA, et al. Karyotypic analysis predicts outcome of preremission and postremission therapy in adult acute myeloid leukemia: a Southwest Oncology Group/Eastern Cooperative Oncology Group study. Blood. 2000;96:4075–4083
  16. Byrd JC, Mrózek K, Dodge RK, et al. Pretreatment cytogenetic abnormalities are predictive of induction success, cumulative incidence of relapse, and overall survival in adult patients with de novo acute myeloid leukemia: results from Cancer and Leukemia Group B (CALGB 8461). Blood. 2002;100:4325–4336
  17. Ferrara F, Palmieri S, Leoni F. Clinically useful prognostic factors in acute myeloid leukemia. Crit Rev Oncol Hematol. 2008;66:181–193
  18. Mrózek K. Cytogenetic, molecular genetic, and clinical characteristics of acute myeloid leukemia with a complex karyotype. Semin Oncol. 2008;35:365–377
  19. Farag SS, Ruppert AS, Mrózek K, et al. Outcome of induction and postremission therapy in younger adults with acute myeloid leukemia with normal karyotype: a Cancer and Leukemia Group B study. J Clin Oncol. 2005;23:482–493
  20. Gaidzik V, Döhner K. Prognostic implications of gene mutations in acute myeloid leukemia with normal cytogenetics. Semin Oncol. 2008;35:346–355
  21. Mrózek K, Marcucci G, Paschka P, et al. 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
  22. Paschka P, Marcucci G, Ruppert AS, et al. Wilms' tumor 1 gene mutations independently predict poor outcome in adults with cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B study. J Clin Oncol. 2008;26:4595–4602
  23. Virappane P, Gale R, Hills R, et al. Mutation of the Wilms' tumor 1 gene is a poor prognostic factor associated with chemotherapy resistance in normal karyotype acute myeloid leukemia: The United Kingdom Medical Research Council Adult Leukaemia Working Party. J Clin Oncol. 2008;26:5429–5435
  24. Marcucci G, Maharry K, Whitman SP, et al. High expression levels of the ETS-related gene, ERG, predict adverse outcome and improve molecular risk-based classification of cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B study. J Clin Oncol. 2007;25:3337–3343
  25. Langer C, Radmacher MD, Ruppert AS, et al. High BAALC expression associates with other molecular prognostic markers, poor outcome, and a distinct gene-expression signature in cytogenetically normal patients younger than 60 years with acute myeloid leukemia: a Cancer and Leukemia Group B (CALGB) study. Blood. 2008;111:5371–5379
  26. 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;108:3898–3905
  27. Langer C, Marcucci G, Holland KB, et al. Prognostic importance of MN1 transcript levels, and biologic insights from MN1-associated gene and microRNA expression signatures in cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B study. J Clin Oncol 2009;27:3198–204.
  28. Döhner K, Schlenk RF, 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
  29. Marcucci G, Maharry K, Radmacher MD, et al. Prognostic significance of, and gene and microRNA expression signatures associated with, CEBPA mutations in cytogenetically normal acute myeloid leukemia with high-risk molecular features: a Cancer and Leukemia Group B study. J Clin Oncol. 2008;26:5078–5087
  30. Paschka P, Marcucci G, Ruppert AS, et al. 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;24:3904–3911
  31. Cairoli R, Beghini A, Grillo G, et al. Prognostic impact of c-KIT mutations in core binding factor leukemias: an Italian retrospective study. Blood. 2006;107:3463–3468
  32. Mrózek K, Marcucci G, Paschka P, et al. Advances in molecular genetics and treatment of core-binding factor acute myeloid leukemia. Curr Opin Oncol. 2008;20:711–718
  33. Wouters BJ, Löwenberg B, Delwel R. A decade of genome-wide gene expression profiling in acute myeloid leukemia: flashback and prospects. Blood. 2009;113:291–298
  34. Bullinger L, Döhner 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
  35. Radmacher MD, Marcucci G, Ruppert AS, 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
  36. Metzeler KH, Hummel M, Bloomfield CD, et al. An 86-probe-set gene-expression signature predicts survival in cytogenetically normal acute myeloid leukemia. Blood. 2008;112:4193–4201
  37. Bullinger L, Rücker FG, Kurz S, et al. Gene-expression profiling identifies distinct subclasses of core binding factor acute myeloid leukemia. Blood. 2007;110:1291–1300
  38. Golub TR, Slonim DK, Tamayo P, et al. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science. 1999;286:531–537
  39. 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
  40. Li Z, Lu J, Sun M, et al. Distinct microRNA expression profiles in acute myeloid leukemia with common translocations. Proc Natl Acad Sci U S A. 2008;105:15535–15540
  41. Dixon-McIver A, East P, Mein CA, et al. Distinctive patterns of microRNA expression associated with karyotype in acute myeloid leukaemia. PLoS ONE. 2008;3:e2141
  42. Jongen-Lavrencic M, Sun SM, Dijkstra MK, et al. MicroRNA expression profiling in relation to the genetic heterogeneity of acute myeloid leukemia. Blood. 2008;111:5078–5085
  43. Garzon R, Volinia S, Liu CG, et al. MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. Blood. 2008;111:3183–3189
  44. Popovic R, Riesbeck LE, Velu CS, et al. Regulation of mir-196b by MLL and its overexpression by MLL fusions contributes to immortalization. Blood. 2009;113:3314–3322
  45. Garzon R, Garofalo M, Martelli MP, et al. Distinctive microRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin. Proc Natl Acad Sci U S A. 2008;105:3945–3950
  46. 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
  47. Verhaak RGW, Goudswaard CS, van Putten W, et al. Mutations in nucleophosmin (NPM1) in acute myeloid leukemia (AML): association with other gene abnormalities and previously established gene expression signatures and their favorable prognostic significance. Blood. 2005;106:3747–3754
  48. O'Connell RM, Rao DS, Chaudhuri AA, et al. Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med. 2008;205:585–594
  49. Hackanson B, Bennett KL, Brena RM, et al. Epigenetic modification of CCAAT/enhancer binding protein α expression in acute myeloid leukemia. Cancer Res. 2008;68:3142–3151
  50. Debernardi S, Skoulakis S, Molloy G, et al. MicroRNA miR-181a correlates with morphological sub-class of acute myeloid leukaemia and the expression of its target genes in global genome-wide analysis. Leukemia. 2007;21:912–916
  51. Isken F, Steffen B, Merk S, et al. Identification of acute myeloid leukaemia associated microRNA expression patterns. Br J Haematol. 2008;140:153–161
  52. Marcucci G, Radmacher MD, Maharry K, et al. MicroRNA expression in cytogenetically normal acute myeloid leukemia. N Engl J Med. 2008;358:1919–1928
  53. Mariathasan S, Monack DM. Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol. 2007;7:31–40
  54. Baltimore D, Boldin MP, O'Connell RM, et al. MicroRNAs: new regulators of immune cell development and function. Nat Immunol. 2008;9:839–845
  55. Taganov KD, Boldin MP, Chang K-J, et al. NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A. 2006;103:12481–12486
  56. Choong ML, Yang HH, McNiece I. MicroRNA expression profiling during human cord blood-derived CD34 cell erythropoiesis. Exp Hematol. 2007;35:551–564
  57. Chiorazzi N, Rai KR, Ferrarini M. Chronic lymphocytic leukemia. N Engl J Med. 2005;352:804–815
  58. Ries LAG, Melbert D, Krapcho M, (eds). SEER cancer statistics review, 1975--2005. Bethesda, MD; National Cancer Institute.Available from: http://seer.cancer.gov/csr/1975_2005/ based on November 2007 SEER data submission, posted to the SEER web site, 2008.
  59. Dighiero G, Hamblin TJ. Chronic lymphocytic leukaemia. Lancet. 2008;371:1017–1029
  60. Nicoloso MS, Kipps TJ, Croce CM, et al. MicroRNAs in the pathogeny of chronic lymphocytic leukaemia. Br J Haematol. 2008;139:709–716
  61. Döhner H, Stilgenbauer S, Benner A, et al. Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med. 2000;343:1910–1916
  62. Stilgenbauer S, Nickolenko J, Wilhelm J, et al. Expressed sequences as candidates for a novel tumor suppressor gene at band 13q14 in B-cell chronic lymphocytic leukemia and mantle cell lymphoma. Oncogene. 1998;16:1891–1897
  63. Elnenaei MO, Hamoudi RA, Swansbury J, et al. Delineation of the minimal region of loss at 13q14 in multiple myeloma. Genes Chromosomes Cancer. 2003;36:99–106
  64. Liu Y, Hermanson M, Grandér D, et al. 13q deletions in lymphoid malignancies. Blood. 1995;86:1911–1915
  65. Yin Z, Spitz MR, Babaian RJ, et al. Limiting the location of a putative human prostate cancer tumor suppressor gene at chromosome 13q14.3. Oncogene. 1999;18:7576–7583
  66. Latil A, Chene L, Mangin P, et al. Extensive analysis of the 13q14 region in human prostate tumors: DNA analysis and quantitative expression of genes lying in the interval of deletion. Prostate. 2003;57:39–50
  67. Pei L, Melmed S, Scheithauer B, et al. Frequent loss of heterozygosity at the retinoblastoma susceptibility gene (RB) locus in aggressive pituitary tumors: evidence for a chromosome 13 tumor suppressor gene other than RB. Cancer Res. 1995;55:1613–1616
  68. Donangelo I, Araújo PB, Antenuzi D, et al. Tumor deletion mapping of chromosomal region 13q14 in 43 growth hormone secreting pituitary adenomas. Endocrine. 2005;28:131–136
  69. Calin GA, Dumitru CD, Shimizu M, et al. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A. 2002;99:15524–15529
  70. Cimmino A, Calin GA, 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
  71. Calin GA, Ferracin M, Cimmino A, et al. A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005;353:1793–1801
  72. Kitada S, Andersen J, Akar S, et al. Expression of apoptosis-regulating proteins in chronic lymphocytic leukemia: correlations with in vitro and in vivo chemoresponses. Blood. 1998;91:3379–3389
  73. Sánchez-Beato M, Sánchez-Aguilera A, Piris MA. Cell cycle deregulation in B-cell lymphomas. Blood. 2003;101:1220–1235
  74. Tsujimoto Y, Finger LR, Yunis J, et al. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science. 1984;226:1097–1099
  75. Tsujimoto Y, Cossman J, Jaffe E, et al. Involvement of the bcl-2 gene in human follicular lymphoma. Science. 1985;228:1440–1443
  76. Adachi M, Tefferi A, Greipp PR, et al. Preferential linkage of bcl-2 to immunoglobulin light chain gene in chronic lymphocytic leukemia. J Exp Med. 1990;171:559–564
  77. Raveche ES, Salerno E, Scaglione BJ, et al. Abnormal microRNA-16 locus with synteny to human 13q14 linked to CLL in NZB mice. Blood. 2007;109:5079–5086
  78. Fabbri M, Garzon R, Cimmino A, et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A. 2007;104:15805–15810
  79. Garzon R, Liu S, Fabbri M, et al. MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene re-expression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood 2009;113:6411--8.
  80. Pekarsky Y, Santanam U, Cimmino A, et al. Tcl1 expression in CLL is regulated by miR-29 and miR-181. Cancer Res. 2006;66:11590–11593
  81. Virgilio L, Narducci MG, Isobe M, et al. Identification of the TCL1 gene involved in T-cell malignancies. Proc Natl Acad Sci U S A. 1994;91:12530–12534
  82. Herling M, Patel KA, Khalili J, et al. TCL1 shows a regulated expression pattern in chronic lymphocytic leukemia that correlates with molecular subtypes and proliferative state. Leukemia. 2006;20:280–285
  83. Hoyer KK, French SW, Turner DE, et al. Dysregulated TCL1 promotes multiple classes of mature B cell lymphoma. Proc Natl Acad Sci U S A. 2002;99:14392–14397
  84. Browning RL, Geyer SM, Johnson AJ, et al. Expression of TCL-1 as a potential prognostic factor for treatment outcome in B-cell chronic lymphocytic leukemia. Leuk Res. 2007;31:1737–1740
  85. Bichi R, Shinton SA, Martin ES, et al. Human chronic lymphocytic leukemia modeled in mouse by targeted TCL1 expression. Proc Natl Acad Sci U S A. 2002;99:6955–6960
  86. Johnson AJ, Lucas DM, Muthusamy N, et al. Characterization of the TCL-1 transgenic mouse as a preclinical drug development tool for human chronic lymphocytic leukemia. Blood. 2006;108:1334–1338
  87. Yang M, Mattes J. Discovery, biology and therapeutic potential of RNA interference, microRNA and antagomirs. Pharmacol Ther. 2008;117:94–104

PII: S1521-6926(09)00028-0

doi: 10.1016/j.beha.2009.05.003

Best Practice & Research Clinical Haematology
Volume 22, Issue 2 , Pages 239-248 , June 2009