Translational implications of somatic genomics in acute myeloid leukaemia

The Lancet Oncology

Volumn 15, Issue 9, 2014, Pages

  Meyer, Sara C ^a   Levine, Ross L ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; CD135 ANTIGEN; COHESIN; DNA; DNA METHYLTRANSFERASE 3A; ISOCITRATE DEHYDROGENASE; MIXED LINEAGE LEUKEMIA PROTEIN; NUCLEOPHOSMIN; ONCOPROTEIN; PROTEIN ASXL1; PROTEIN P53; PROTEIN PHF6; PROTEIN TET2; RAS PROTEIN; STEM CELL FACTOR RECEPTOR; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG; WT1 PROTEIN; ANTINEOPLASTIC AGENT; CCAAT ENHANCER BINDING PROTEIN; CEBPA PROTEIN, HUMAN; NUCLEAR PROTEIN;

ACUTE GRANULOCYTIC LEUKEMIA; CANCER CLASSIFICATION; CANCER PROGNOSIS; CARCINOGENESIS; CEPRA GENE; CHROMOSOME ABERRATION; CHROMOSOME INVERSION; COHESIN GENE; DNA SEQUENCE; DNMT3A GENE; FLT3 GENE; GENE IDENTIFICATION; GENE MUTATION; GENE TRANSLOCATION; GENETIC ASSOCIATION; GENOMICS; HUMAN; KIT GENE; MLL GENE; MOLECULAR CLONING; NEXT GENERATION SEQUENCING; NONHUMAN; NPM1 GENE; ONCOGENE; ONCOGENE RAS; PHF6 GENE; PRIORITY JOURNAL; REVIEW; RUNX1 GENE; SPLICEOSOME; TET2 GENE; TP53 GENE; TRANSLATION REGULATION; WT1 GENE; ADULT; ALLELE; EPIDEMIOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETIC SCREENING; GENETICS; LEUKEMIA, MYELOID, ACUTE; MALE; MORTALITY; MUTATION; NUCLEOTIDE SEQUENCE; PROCEDURES; PROGNOSIS; RISK ASSESSMENT; SURVIVAL; TREATMENT OUTCOME;

ADULT; ALLELES; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CCAAT-ENHANCER-BINDING PROTEINS; DNA MUTATIONAL ANALYSIS; FEMALE; FMS-LIKE TYROSINE KINASE 3; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC PREDISPOSITION TO DISEASE; GENETIC TESTING; GENOMICS; HUMANS; LEUKEMIA, MYELOID, ACUTE; MALE; MUTATION; NUCLEAR PROTEINS; PROGNOSIS; RISK ASSESSMENT; SEQUENCE ANALYSIS, DNA; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 84904903686     PISSN: 14702045     EISSN: 14745488     Source Type: Journal    
DOI: 10.1016/S1470-2045(14)70008-7     Document Type: Review

References (85)

1. Gregory TK, Wald D, Chen Y, Vermaat JM, Xiong Y, Tse W Molecular prognostic markers for adult acute myeloid leukemia with normal cytogenetics. J Hematol Oncol 2009, 2:23.
2. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med 2013, 368:2059-2074. Cancer Genome Atlas Research Network.
3. Patel JP, Gönen M, Figueroa ME, et al. Prognostic relevance of integrated genetic profiling in acute myeloid leukemia. N Engl J Med 2012, 366:1079-1089.
4. Döhner H, Estey EH, Amadori S, et al. Diagnosis and management of acute myeloid leukemia in adults: recommendations from an international expert panel, on behalf of the European LeukemiaNet. Blood 2010, 115:453-474. the European LeukemiaNet.
5. Lo-Coco F, Avvisati G, Vignetti M, et al. Retinoic acid and arsenic trioxide for acute promyelocytic leukemia. N Engl J Med 2013, 369:111-121. the Gruppo Italiano Malattie Ematologiche dell'Adulto, the German-Austrian Acute Myeloid Leukemia Study Groupthe German-Austrian Acute Myeloid Leukemia Study Group, the Study Alliance Leukemiathe Study Alliance Leukemia.
6. Byrd JC, Dodge RK, Carroll A, et al. Patients with t(8;21)(q22;q22) and acute myeloid leukemia have superior failure-free and overall survival when repetitive cycles of high-dose cytarabine are administered. J Clin Oncol 1999, 17:3767-3775.
7. Bernt KM, Armstrong SA Targeting epigenetic programs in MLL-rearranged leukemias. Hematology Am Soc Hematol Educ Program 2011, 3:354-360.
8. Bernt KM, Zhu N, Sinha AU, et al. MLL-rearranged leukemia is dependent on aberrant H3K79 methylation by DOT1L. Cancer Cell 2011, 20:66-78.
9. Rucker FG, Bullinger L, Schwaenen C, et al. Disclosure of candidate genes in acute myeloid leukemia with complex karyotypes using microarray-based molecular characterization. J Clin Oncol 2006, 24:3887-3894.
10. Bowen D, Groves MJ, Burnett AK, et al. TP53 gene mutation is frequent in patients with acute myeloid leukemia and complex karyotype, and is associated with very poor prognosis. Leukemia 2009, 23:203-206.
11. Breems DA, Van Putten WL, De Greef GE, et al. Monosomal karyotype in acute myeloid leukemia: a better indicator of poor prognosis than a complex karyotype. J Clin Oncol 2008, 26:4791-4797.
12. Slovak ML, Gundacker H, Bloomfield CD, et al. A retrospective study of 69 patients with t(6;9)(p23;q34) AML emphasizes the need for a prospective, multicenter initiative for rare 'poor prognosis' myeloid malignancies. Leukemia 2006, 20:1295-1297.
13. Walter MJ, Payton JE, Ries RE, et al. Acquired copy number alterations in adult acute myeloid leukemia genomes. Proc Natl Acad Sci USA 2009, 106:12950-12955.
14. Welch JS, Westervelt P, Ding L, et al. Use of whole-genome sequencing to diagnose a cryptic fusion oncogene. JAMA 2011, 305:1577-1584.
15. Schlenk RF, Döhner K, Krauter J, et al. Mutations and treatment outcome in cytogenetically normal acute myeloid leukemia. N Engl J Med 2008, 358:1909-1918. the German-Austrian Acute Myeloid Leukemia Study Group.
16. Marcucci G, Haferlach T, Dohner H Molecular genetics of adult acute myeloid leukemia: prognostic and therapeutic implications. J Clin Oncol 2011, 29:475-486.
17. Paschka P, Schlenk RF, Gaidzik VI, et al. IDH1 and IDH2 mutations are frequent genetic alterations in acute myeloid leukemia and confer adverse prognosis in cytogenetically normal acute myeloid leukemia with NPM1 mutation without FLT3 internal tandem duplication. J Clin Oncol 2010, 28:3636-3643.
18. Kayser S, Schlenk RF, Londono MC, et al. Insertion of FLT3 internal tandem duplication in the tyrosine kinase domain-1 is associated with resistance to chemotherapy and inferior outcome. Blood 2009, 114:2386-2392. the German-Austrian AML Study Group (AMLSG).
19. Schnittger S, Bacher U, Kern W, Alpermann T, Haferlach C, Haferlach T Prognostic impact of FLT3-ITD load in NPM1 mutated acute myeloid leukemia. Leukemia 2011, 25:1297-1304.
20. Sengsayadeth SM, Jagasia M, Engelhardt BG, et al. Allo-SCT for high-risk AML-CR1 in the molecular era: impact of FLT3/ITD outweighs the conventional markers. Bone Marrow Transplant 2012, 47:1535-1537.
21. Mead AJ, Linch DC, Hills RK, Wheatley K, Burnett AK, Gale RE FLT3 tyrosine kinase domain mutations are biologically distinct from and have a significantly more favorable prognosis than FLT3 internal tandem duplications in patients with acute myeloid leukemia. Blood 2007, 110:1262-1270.
22. Whitman SP, Ruppert AS, Radmacher MD, et al. FLT3 D835/I836 mutations are associated with poor disease-free survival and a distinct gene-expression signature among younger adults with de novo cytogenetically normal acute myeloid leukemia lacking FLT3 internal tandem duplications. Blood 2008, 111:1552-1559.
23. Ozeki K, Kiyoi H, Hirose Y, et al. Biologic and clinical significance of the FLT3 transcript level in acute myeloid leukemia. Blood 2004, 103:1901-1908.
24. Mead AJ, Gale RE, Kottaridis PD, Matsuda S, Khwaja A, Linch DC Acute myeloid leukaemia blast cells with a tyrosine kinase domain mutation of FLT3 are less sensitive to lestaurtinib than those with a FLT3 internal tandem duplication. Br J Haematol 2008, 141:454-460.
25. Stone RM, Fischer T, Paquette R, et al. Phase IB study of the FLT3 kinase inhibitor midostaurin with chemotherapy in younger newly diagnosed adult patients with acute myeloid leukemia. Leukemia 2012, 26:2061-2068.
26. Pabst T, Mueller BU, 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.
27. Wouters BJ, Löwenberg B, Erpelinck-Verschueren CA, van Putten WL, Valk PJ, Delwel R Double CEBPA mutations, but not single CEBPA mutations, define a subgroup of acute myeloid leukemia with a distinctive gene expression profile that is uniquely associated with a favorable outcome. Blood 2009, 113:3088-3091.
28. Schubbert S, Shannon K, Bollag G Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 2007, 7:295-308.
29. Schnittger S, Kinkelin U, Schoch C, et al. Screening for MLL tandem duplication in 387 unselected patients with AML identify a prognostically unfavorable subset of AML. Leukemia 2000, 14:796-804.
30. Whitman SP, Ruppert AS, Marcucci G, et al. Long-term disease-free survivors with cytogenetically normal acute myeloid leukemia and MLL partial tandem duplication: a Cancer and Leukemia Group B study. Blood 2007, 109:5164-5167.
31. King-Underwood L, Pritchard-Jones K Wilms' tumor (WT1) gene mutations occur mainly in acute myeloid leukemia and may confer drug resistance. Blood 1998, 91:2961-2968.
32. Gaidzik VI, Bullinger L, Schlenk RF, et al. RUNX1 mutations in acute myeloid leukemia: results from a comprehensive genetic and clinical analysis from the AML study group. J Clin Oncol 2011, 29:1364-1372.
33. 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.
34. Kindler T, Breitenbuecher F, Marx A, et al. Efficacy and safety of imatinib in adult patients with c-kit-positive acute myeloid leukemia. Blood 2004, 103:3644-3654.
35. Rücker FG, Schlenk RF, Bullinger L, et al. TP53 alterations in acute myeloid leukemia with complex karyotype correlate with specific copy number alterations, monosomal karyotype, and dismal outcome. Blood 2012, 119:2114-2121.
36. Yuan Y, Zhou L, Miyamoto T, et al. AML1-ETO expression is directly involved in the development of acute myeloid leukemia in the presence of additional mutations. Proc Natl Acad Sci USA 2001, 98:10398-10403.
37. Song WJ, Sullivan MG, Legare RD, et al. Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat Genet 1999, 23:166-175.
38. Bochtler T, Stolzel F, Heilig CE, et al. Clonal heterogeneity as detected by metaphase karyotyping is an indicator of poor prognosis in acute myeloid leukemia. J Clin Oncol 2013, 31:3898-3905.
39. Kern W, Haferlach T, Schnittger S, Ludwig WD, Hiddemann W, Schoch C Karyotype instability between diagnosis and relapse in 117 patients with acute myeloid leukemia: implications for resistance against therapy. Leukemia 2002, 16:2084-2091.
40. Ding L, Ley TJ, Larson DE, et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012, 481:506-510.
41. Ley TJ, Mardis ER, Ding L, et al. DNA sequencing of a cytogenetically normal acute myeloid leukaemia genome. Nature 2008, 456:66-72.
42. Mardis ER, Ding L, Dooling DJ, et al. Recurring mutations found by sequencing an acute myeloid leukemia genome. N Engl J Med 2009, 361:1058-1066.
43. Ley TJ, Ding L, Walter MJ, et al. DNMT3A mutations in acute myeloid leukemia. N Engl J Med 2010, 363:2424-2433.
44. Fried I, Bodner C, Pichler MM, et al. Frequency, onset and clinical impact of somatic DNMT3A mutations in therapy-related and secondary acute myeloid leukemia. Haematologica 2012, 97:246-250.
45. Challen GA, Sun D, Jeong M, et al. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat Genet 2012, 44:23-31.
46. Ward PS, Patel J, Wise DR, et al. The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell 2010, 17:225-234.
47. Thol F, Damm F, Wagner K, et al. Prognostic impact of IDH2 mutations in cytogenetically normal acute myeloid leukemia. Blood 2010, 116:614-616.
48. Figueroa ME, Abdel-Wahab O, Lu C, et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 2010, 18:553-567.
49. Delhommeau F, Dupont S, Della Valle V, et al. Mutation in TET2 in myeloid cancers. N Engl J Med 2009, 360:2289-2301.
50. Moran-Crusio K, Reavie L, Shih A, et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 2011, 20:11-24.
51. Gelsi-Boyer V, Trouplin V, Adélaïde J, et al. Mutations of polycomb-associated gene ASXL1 in myelodysplastic syndromes and chronic myelomonocytic leukaemia. Br J Haematol 2009, 145:788-800.
52. Metzeler KH, Becker H, Maharry K, et al. ASXL1 mutations identify a high-risk subgroup of older patients with primary cytogenetically normal AML within the ELN Favorable genetic category. Blood 2011, 118:6920-6929.
53. Abdel-Wahab O, Adli M, LaFave LM, et al. ASXL1 mutations promote myeloid transformation through loss of PRC2-mediated gene repression. Cancer Cell 2012, 22:180-193.
54. Van Vlierberghe P, Patel J, Abdel-Wahab O, et al. PHF6 mutations in adult acute myeloid leukemia. Leukemia 2011, 25:130-134.
55. Solomon DA, Kim T, Diaz-Martinez LA, et al. Mutational inactivation of STAG2 causes aneuploidy in human cancer. Science 2011, 333:1039-1043.
56. Welch JS, Ley TJ, Link DC, et al. The origin and evolution of mutations in acute myeloid leukemia. Cell 2012, 150:264-278.
57. Wang L, Lawrence MS, Wan Y, et al. SF3B1 and other novel cancer genes in chronic lymphocytic leukemia. N Engl J Med 2011, 365:2497-2506.
58. Yoshida K, Sanada M, Shiraishi Y, et al. Frequent pathway mutations of splicing machinery in myelodysplasia. Nature 2011, 478:64-69.
59. Papaemmanuil E, Cazzola M, Boultwood J, et al. Somatic SF3B1 mutation in myelodysplasia with ring sideroblasts. N Engl J Med 2011, 365:1384-1395. the Chronic Myeloid Disorders Working Group of the International Cancer Genome Consortium.
60. Lasho TL, Jimma T, Finke CM, et al. SRSF2 mutations in primary myelofibrosis: significant clustering with IDH mutations and independent association with inferior overall and leukemia-free survival. Blood 2012, 120:4168-4171.
61. Maciejewski JP, Padgett RA Defects in spliceosomal machinery: a new pathway of leukaemogenesis. Br J Haematol 2012, 158:165-173.
62. 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.
63. Marcucci G, Maharry K, Wu YZ, et al. IDH1 and IDH2 gene mutations identify novel molecular subsets within de novo cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B study. J Clin Oncol 2010, 28:2348-2355.
64. Metzeler KH, Dufour A, Benthaus T, et al. ERG expression is an independent prognostic factor and allows refined risk stratification in cytogenetically normal acute myeloid leukemia: a comprehensive analysis of ERG, MN1, and BAALC transcript levels using oligonucleotide microarrays. J Clin Oncol 2009, 27:5031-5038.
65. 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.
66. Figueroa ME, Lugthart S, Li Y, et al. DNA methylation signatures identify biologically distinct subtypes in acute myeloid leukemia. Cancer Cell 2010, 17:13-27.
67. Valk PJ, Verhaak RG, Beijen MA, et al. Prognostically useful gene-expression profiles in acute myeloid leukemia. N Engl J Med 2004, 350:1617-1628.
68. Lin P, Hao S, Medeiros LJ, et al. Expression of CD2 in acute promyelocytic leukemia correlates with short form of PML-RARalpha transcripts and poorer prognosis. Am J Clin Pathol 2004, 121:402-407.
69. Mi S, Lu J, Sun M, et al. MicroRNA expression signatures accurately discriminate acute lymphoblastic leukemia from acute myeloid leukemia. Proc Natl Acad Sci USA 2007, 104:19971-19976.
70. 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.
71. Garzon R, Volinia S, Liu CG, et al. MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. Blood 2008, 111:3183-3189.
72. Krivtsov AV, Feng Z, Lemieux ME, et al. H3K79 methylation profiles define murine and human MLL-AF4 leukemias. Cancer Cell 2008, 14:355-368.
73. Rombouts EJ, Pavic B, Löwenberg B, Ploemacher RE Relation between CXCR-4 expression, Flt3 mutations, and unfavorable prognosis of adult acute myeloid leukemia. Blood 2004, 104:550-557.
74. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 2006, 12:1167-1174.
75. Matsunaga T, Takemoto N, Sato T, et al. Interaction between leukemic-cell VLA-4 and stromal fibronectin is a decisive factor for minimal residual disease of acute myelogenous leukemia. Nat Med 2003, 9:1158-1165.
76. Kronke J, Schlenk RF, Jensen KO, et al. Monitoring of minimal residual disease in NPM1-mutated acute myeloid leukemia: a study from the German-Austrian acute myeloid leukemia study group. J Clin Oncol 2011, 29:2709-2716.
77. Schnittger S, Kern W, Tschulik C, et al. Minimal residual disease levels assessed by NPM1 mutation-specific RQ-PCR provide important prognostic information in AML. Blood 2009, 114:2220-2231.
78. Cilloni D, Renneville A, Hermitte F, et al. Real-time quantitative polymerase chain reaction detection of minimal residual disease by standardized WT1 assay to enhance risk stratification in acute myeloid leukemia: a European LeukemiaNet study. J Clin Oncol 2009, 27:5195-5201.
79. Kristensen T, Møller MB, Friis L, Bergmann OJ, Preiss B NPM1 mutation is a stable marker for minimal residual disease monitoring in acute myeloid leukaemia patients with increased sensitivity compared to WT1 expression. Eur J Haematol 2011, 87:400-408.
80. Weisser M, Kern W, Schoch C, Hiddemann W, Haferlach T, Schnittger S Risk assessment by monitoring expression levels of partial tandem duplications in the MLL gene in acute myeloid leukemia during therapy. Haematologica 2005, 90:881-889.
81. Freeman SD, Virgo P, Couzens S, et al. Prognostic relevance of treatment response measured by flow cytometric residual disease detection in older patients with acute myeloid leukemia. J Clin Oncol 2013, 31:4123-4131.
82. Steensma DP The beginning of the end of the beginning in cancer genomics. N Engl J Med 2013, 368:2138-2140.
83. Hartford CM, Duan S, Delaney SM, et al. Population-specific genetic variants important in susceptibility to cytarabine arabinoside cytotoxicity. Blood 2009, 113:2145-2153.
84. Naoe T, Tagawa Y, Kiyoi H, et al. Prognostic significance of the null genotype of glutathione S-transferase-T1 in patients with acute myeloid leukemia: increased early death after chemotherapy. Leukemia 2002, 16:203-208.
85. Nickels EM, Soodalter J, Churpek JE, Godley LA Recognizing familial myeloid leukemia in adults. Ther Adv Hematol 2013, 4:254-269.