Tumor heterogeneity makes AML a "moving target" for detection of residual disease

Cytometry Part B - Clinical Cytometry

Volumn 86, Issue 1, 2014, Pages 3-14

  Zeijlemaker, W ^a   Gratama, J W ^b   Schuurhuis, G J ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

acute myeloid leukemia; clonal evolution; flow cytometry; minimal residual disease; phenotypic changes; quantitative polymerase chain reaction

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; FLT3 LIGAND; NUCLEOPHOSMIN; PROTEIN P53; RAS PROTEIN; WT1 PROTEIN;

ACUTE GRANULOCYTIC LEUKEMIA; ANTIGEN EXPRESSION; CANCER CELL POPULATION HETEROGENEITY; CANCER GENETICS; CANCER PROGNOSIS; CANCER RISK; CHROMOSOME ABERRATION; CHROMOSOME INVERSION; CHROMOSOME TRANSLOCATION; CLONAL EVOLUTION; CYTOGENETICS; GENE MUTATION; GENOME; HUMAN; IMMUNOPHENOTYPING; MINIMAL RESIDUAL DISEASE; NEOPLASM; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT;

ACUTE MYELOID LEUKEMIA; CLONAL EVOLUTION; FLOW CYTOMETRY; MINIMAL RESIDUAL DISEASE; PHENOTYPIC CHANGES; QUANTITATIVE POLYMERASE CHAIN REACTION;

ADULT; CLONAL EVOLUTION; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; GENETIC VARIATION; HUMANS; IMMUNOPHENOTYPING; LEUKEMIA, MYELOID, ACUTE; NEOPLASM RECURRENCE, LOCAL; NEOPLASM, RESIDUAL; REAL-TIME POLYMERASE CHAIN REACTION; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84890546828     PISSN: 15524949     EISSN: 15524957     Source Type: Journal    
DOI: 10.1002/cyto.b.21134     Document Type: Review

References (93)

1. Cornelissen JJ, van Putten WLJ, Verdonck LF, Theobald M, Jacky E, Daenen SMG, van Marwijk Kooy M, Wijermans P, Schouten H, Huijgens PC, van der Lelie H, Fey M, Ferrant A, Maertens J, Gratwohl A, Lowenberg B,. Results of a HOVON/SAKK donor versus no-donor analysis of myeloablative HLA-identical sibling stem cell transplantation in first remission acute myeloid leukemia in young and middle-aged adults: Benefits for whom? Blood 2007; 109: 3658-3666.
2. San Miguel JF, Martínez a, Macedo a, Vidriales MB, Lõpez-Berges C, González M, Caballero D, García-Marcos M a, Ramos F, Fernández-Calvo J, Calmuntia MJ, Diaz-Mediavilla J, Orfao A,. Immunophenotyping investigation of minimal residual disease is a useful approach for predicting relapse in acute myeloid leukemia patients. Blood 1997; 90: 2465-2470.
3. San Miguel JF, Vidriales MB, Lõpez-Berges C, Díaz-Mediavilla J, Gutiérrez N, Cañizo C, Ramos F, Calmuntia MJ, Pérez JJ, González M, Orfao A,. Early immunophenotypical evaluation of minimal residual disease in acute myeloid leukemia identifies different patient risk groups and may contribute to postinduction treatment stratification. Blood 2001; 98: 1746-1751.
4. Kern W, Voskova D, Schoch C, Hiddemann W, Schnittger S, Haferlach T,. Determination of relapse risk based on assessment of minimal residual disease during complete remission by multiparameter flow cytometry in unselected patients with acute myeloid leukemia. Blood 2004; 104: 3078-3085.
5. Feller N, van der Pol M a, van Stijn A, Weijers GWD, Westra a H, Evertse BW, Ossenkoppele GJ, Schuurhuis GJ,. MRD parameters using immunophenotypic detection methods are highly reliable in predicting survival in acute myeloid leukaemia. Leukemia 2004; 18: 1380-1390.
6. Venditti A, Buccisano F, Del Poeta G, Maurillo L, Tamburini A, Cox C, Battaglia A, Catalano G, Del Moro B, Cudillo L, Postorino M, Masi M, Amadori S,. Level of minimal residual disease after consolidation therapy predicts outcome in acute myeloid leukemia: Presented in part at the 41st Annual Meeting of the American Society of Hematology, December 3-7, 1999, New Orleans, LA. Blood 2000; 96: 3948-3952.
7. Maurillo L, Buccisano F, Del Principe MI, Del Poeta G, Spagnoli A, Panetta P, Ammatuna E, Neri B, Ottaviani L, Sarlo C, Venditti D, Quaresima M, Cerretti R, Rizzo M, de Fabritiis P, Lo Coco F, Arcese W, Amadori S, Venditti A,. Toward optimization of postremission therapy for residual disease-positive patients with acute myeloid leukemia. J Clin Oncol 2008; 26: 4944-4951.
8. Díez-Campelo M, Pérez-Simõn JA, Pérez J, Alcoceba M, Richtmon J, Vidriales B, San Miguel J,. Minimal residual disease monitoring after allogeneic transplantation may help to individualize post-transplant therapeutic strategies in acute myeloid malignancies. Am J Hematol 2009; 84: 149-152.
9. Al-Mawali A, Gillis D, Lewis I,. The use of receiver operating characteristic analysis for detection of minimal residual disease using five-color multiparameter flow cytometry in acute myeloid leukemia identifies patients with high risk of relapse. Cytometry B Clin Cytom 2009; 76B: 91-101.
10. Ossenkoppele GJ, van de Loosdrecht AA, Schuurhuis GJ,. Review of the relevance of aberrant antigen expression by flow cytometry in myeloid neoplasms. Br J Haematol 2011; 153: 421-36.
11. Sugimoto T, Das H, Imoto S, Murayama T, Gomyo H, Chakraborty S, Taniguchi R, Isobe T, Nakagawa T, Nishimura R, Koizumi T,. Quantitation of minimal residual disease in t(8;21)-positive acute myelogenous leukemia patients using real-time quantitative RT-PCR. Am J Hematol 2000; 64: 101-106.
12. Guerrasio A, Pilatrino C, De Micheli D, Cilloni D, Serra A, Gottardi E, Parziale A, Marmont F, Diverio D, Divona M, Lo Coco F, Saglio G,. Assessment of minimal residual disease (MRD) in CBFbeta/MYH11-positive acute myeloid leukemias by qualitative and quantitative RT-PCR amplification of fusion transcripts. Leukemia 2002; 16: 1176-1181.
13. Papadaki C, Dufour A, Seibl M, Schneider S, Bohlander SK, Zellmeier E, Mellert G, Hiddemann W, Spiekermann K,. Monitoring minimal residual disease in acute myeloid leukaemia with NPM1 mutations by quantitative PCR: Clonal evolution is a limiting factor. Br J Haematol 2009; 144: 517-523.
14. Tobal K, Yin J a,. Monitoring of minimal residual disease by quantitative reverse transcriptase-polymerase chain reaction for AML1-MTG8 transcripts in AML-M2 with t(8; 21). Blood 1996; 88: 3704-3709.
15. Mitterbauer G, Zimmer C, Pirc-Danoewinata H, Haas O a, Hojas S, Schwarzinger I, Greinix H, Jäger U, Lechner K, Mannhalter C,. Monitoring of minimal residual disease in patients with MLL-AF6-positive acute myeloid leukaemia by reverse transcriptase polymerase chain reaction. Br J Haematol 2000; 109: 622-628.
16. Chou W-C, Hou H, Liu C-Y, Chen C-Y, Lin L-I, Huang Y-N, Chao Y-C, Hsu C, Huang C-F, Tien H-F,. Sensitive measurement of quantity dynamics of FLT3 internal tandem duplication at early time points provides prognostic information. Ann Oncol 2011; 22: 696-704.
17. Barragan E, Pajuelo JC, Ballester S, Fuster O, Cervera J, Moscardo F, Senent L, Such E, Sanz M a, Bolufer P,. Minimal residual disease detection in acute myeloid leukemia by mutant nucleophosmin (NPM1): Comparison with WT1 gene expression. Clin Chim Acta 2008; 395: 120-123.
18. Terstappen LW, Loken MR,. Myeloid cell differentiation in normal bone marrow and acute myeloid leukemia assessed by multi-dimensional flow cytometry. Anal Cell Pathol 1990; 2: 229-240.
19. Terstappen LW, Safford M, Könemann S, Loken MR, Zurlutter K, Büchner T, Hiddemann W, Wörmann B,. Flow cytometric characterization of acute myeloid leukemia. Part II. Phenotypic heterogeneity at diagnosis. Leukemia 1992; 6: 70-80.
20. Reading CL, Estey EH, Huh YO, Claxton DF, Sanchez G, Terstappen LW, O'Brien MC, Baron S, Deisseroth a B,. Expression of unusual immunophenotype combinations in acute myelogenous leukemia. Blood 1993; 81: 3083-3090.
21. Terstappen LW, Safford M, Unterhalt M, Könemann S, Zurlutter K, Piechotka K, Drescher M, Aul C, Büchner T, Hiddemann W,. Flow cytometric characterization of acute myeloid leukemia: IV. Comparison to the differentiation pathway of normal hematopoietic progenitor cells. Leukemia 1992; 6: 993-1000.
22. Schnittger S, Kern W, Tschulik C, Weiss T, Dicker F, Falini B, Haferlach C, Haferlach T,. Minimal residual disease levels assessed by NPM1 mutation-specific RQ-PCR provide important prognostic information in AML. Blood 2009; 114: 2220-2231.
23. Sievers EL, Lange BJ, Alonzo T a, Gerbing RB, Bernstein ID, Smith FO, Arceci RJ, Woods WG, Loken MR,. Immunophenotypic evidence of leukemia after induction therapy predicts relapse: results from a prospective Children's Cancer Group study of 252 patients with acute myeloid leukemia. Blood 2003; 101: 3398-3406.
24. Sievers EL, Lange BJ, Buckley JD, Smith FO, Wells DA, Daigneault-creech CA, Shultsjrwind KE, Loken MR,. Prediction of relapse of pediatric acute myeloid leukemia by use of multidimensional flow cytometry flow study patients. J Natl Cancer Inst 1996; 88: 1483-1488.
25. Loken MR, Alonzo TA, Pardo L, Gerbing RB, Raimondi SC, Hirsch BA, Ho PA, Franklin J, Cooper TM, Gamis AS, Meshinchi S,. Residual disease detected by multidimensional flow cytometry signifies high relapse risk in patients with de novo acute myeloid leukemia: A report from Children's Oncology Group. Blood 2012; 120: 1581-1588.
26. Van der Velden VHJ, van der Sluijs-Geling A, Gibson BES, te Marvelde JG, Hoogeveen PG, Hop WCJ, Wheatley K, Bierings MB, Schuurhuis GJ, de Graaf SSN, van Wering ER, van Dongen JJM,. Clinical significance of flowcytometric minimal residual disease detection in pediatric acute myeloid leukemia patients treated according to the DCOG ANLL97/MRC AML12 protocol. Leukemia 2010; 24: 1599-1606.
27. Dimov ND, Medeiros LJ, Ravandi F, Bueso-Ramos CE,. Acute promyelocytic leukemia at time of relapse commonly demonstrates cytogenetic evidence of clonal evolution and variability in blast immunophenotypic features. Am J Clin Pathol 2010; 133: 484-490.
28. Li X, Du W, Liu W, Li X, Li H, Huang S-A,. Comprehensive flow cytometry phenotype in acute leukemia at diagnosis and at relapse. APMIS 2010; 118: 353-359.
29. Macedo A, San Miguel JF, Vidriales MB, Lõpez-Berges MC, García-Marcos MA, Gonzalez M, Landolfi C, Orfão A,. Phenotypic changes in acute myeloid leukaemia: implications in the detection of minimal residual disease. J Clin Pathol 1996; 49: 15-18.
30. Hur M, Chang YH, Lee DS, Park MH, Cho HI,. Immunophenotypic and cytogenetic changes in acute leukaemia at relapse. Clin Lab Haematol 2001; 23: 173-179.
31. Langebrake C, Brinkmann I, Teigler-Schlegel A, Creutzig U, Griesinger F, Puhlmann U, Reinhardt D,. Immunophenotypic differences between diagnosis and relapse in childhood AML: Implications for MRD monitoring. Cytometry B Clin Cytom 2005; 63B: 1-9.
32. Baer MR, Stewart CC, Dodge RK, Leget G, Sule N, Mrõzek K, Schiffer CA, Powell BL, Kolitz JE, Moore JO, Stone RM, Davey FR, Carroll AJ, Larson RA, Bloomfield CD,. High frequency of immunophenotype changes in acute myeloid leukemia at relapse: Implications for residual disease detection (Cancer and Leukemia Group B Study 8361). Blood 2001; 97: 3574-3580.
33. Voskova D, Schoch C, Schnittger S, Hiddemann W, Haferlach T, Kern W,. Stability of leukemia-associated aberrant immunophenotypes in patients with acute myeloid leukemia between diagnosis and relapse: comparison with cytomorphologic, cytogenetic, and molecular genetic findings. Cytometry B Clin Cytom 2004; 62B: 25-38.
34. Grimwade D, Jovanovic J V, Hills RK, Nugent E a, Patel Y, Flora R, Diverio D, Jones K, Aslett H, Batson E, Rennie K, Angell R, Clark RE, Solomon E, Lo-Coco F, Wheatley K, Burnett AK,. Prospective minimal residual disease monitoring to predict relapse of acute promyelocytic leukemia and to direct pre-emptive arsenic trioxide therapy. J Clin Oncol 2009; 27: 3650-3658.
35. Krauter J, Gorlich K, Ottmann O, Lubbert M, Dohner H, Heit W, Kanz L, Ganser A, Heil G,. Prognostic value of minimal residual disease quantification by real-time reverse transcriptase polymerase chain reaction in patients with core binding factor leukemias. J Clin Oncol 2003; 21: 4413-4422.
36. Cilloni D, Renneville A, Hermitte F, Hills RK, Daly S, Jovanovic J V, Gottardi E, Fava M, Schnittger S, Weiss T, Izzo B, Nomdedeu J, van der Heijden A, van der Reijden B a, Jansen JH, van der Velden VHJ, Ommen H, Preudhomme C, Saglio G, Grimwade D,. 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.
37. Buonamici S,. Real-time quantitation of minimal residual disease in inv(16)-positive acute myeloid leukemia may indicate risk for clinical relapse and may identify patients in a curable state. Blood 2002; 99: 443-449.
38. 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.
39. Schmidt-Hieber M, Blau IW, Richter G, Türkmen S, Bommer C, Thiel G, Neitzel H, Stroux A, Uharek L, Thiel E, Blau O,. Cytogenetic studies in acute leukemia patients relapsing after allogeneic stem cell transplantation. Cancer Genet Cytogenet 2010; 198: 135-143.
40. Schnittger S,. Analysis of FLT3 length mutations in 1003 patients with acute myeloid leukemia: correlation to cytogenetics, FAB subtype, and prognosis in the AMLCG study and usefulness as a marker for the detection of minimal residual disease. Blood 2002; 100: 59-66.
41. Cloos J, Goemans BF, Hess CJ, van Oostveen JW, Waisfisz Q, Corthals S, de Lange D, Boeckx N, Hählen K, Reinhardt D, Creutzig U, Schuurhuis GJ, Zwaan CM, Kaspers GJL,. Stability and prognostic influence of FLT3 mutations in paired initial and relapsed AML samples. Leukemia 2006; 20: 1217-1220.
42. Kottaridis PD, Gale RE, Langabeer SE, Frew ME, Bowen DT, Linch DC,. Studies of FLT3 mutations in paired presentation and relapse samples from patients with acute myeloid leukemia: Implications for the role of FLT3 mutations in leukemogenesis, minimal residual disease detection, and possible therapy with FLT3 inhibitors. Blood 2002; 100: 2393-2398.
43. Bachas C, Schuurhuis GJ, Hollink IHIM, Kwidama ZJ, Goemans BF, Zwaan CM, van den Heuvel-Eibrink MM, de Bont ESJM, Reinhardt D, Creutzig U, de Haas V, Assaraf YG, Kaspers GJL, Cloos J,. High-frequency type I/II mutational shifts between diagnosis and relapse are associated with outcome in pediatric AML: Implications for personalized medicine. Blood 2010; 116: 2752-2758.
44. Schiller J, Praulich I, Krings Rocha C, Kreuzer K-A,. Patient-specific analysis of FLT3 internal tandem duplications for the prognostication and monitoring of acute myeloid leukemia. Eur J Haematol 2012; 89: 53-62.
45. Warren M, Luthra R, Yin CC, Ravandi F, Cortes JE, Kantarjian HM, Medeiros LJ, Zuo Z,. Clinical impact of change of FLT3 mutation status in acute myeloid leukemia patients. Mod Pathol 2012; 25: 1405-1412.
46. Suzuki T, Kiyoi H, Ozeki K, Tomita A, Yamaji S, Suzuki R, Kodera Y, Miyawaki S, Asou N, Kuriyama K, Yagasaki F, Shimazaki C, Akiyama H, Nishimura M, Motoji T, Shinagawa K, Takeshita A, Ueda R, Kinoshita T, Emi N, Naoe T,. Clinical characteristics and prognostic implications of NPM1 mutations in acute myeloid leukemia. Blood 2005; 106: 2854-2861.
47. Hollink IHIM, van den Heuvel-Eibrink MM, Zimmermann M, Balgobind B V, Arentsen-Peters STCJM, Alders M, Willasch A, Kaspers GJL, Trka J, Baruchel A, de Graaf SSN, Creutzig U, Pieters R, Reinhardt D, Zwaan CM,. Clinical relevance of Wilms tumor 1 gene mutations in childhood acute myeloid leukemia. Blood 2009; 113: 5951-5960.
48. Hou H-A, Huang T-C, Lin L-I, Liu C-Y, Chen C-Y, Chou W-C, Tang J-L, Tseng M-H, Huang C-F, Chiang Y-C, Lee F-Y, Liu M-C, Yao M, Huang S-Y, Ko B-S, Hsu S-C, Wu S-J, Tsay W, Chen Y-C, Tien H-F,. WT1 mutation in 470 adult patients with acute myeloid leukemia: stability during disease evolution and implication of its incorporation into a survival scoring system. Blood 2010; 115: 5222-5231.
49. Chou W-C, Tang J-L, Wu S-J, Tsay W, Yao M, Huang S-Y, Huang K-C, Chen C-Y, Huang C-F, Tien H-F,. Clinical implications of minimal residual disease monitoring by quantitative polymerase chain reaction in acute myeloid leukemia patients bearing nucleophosmin (NPM1) mutations. Leukemia 2007; 21: 998-1004.
50. Haferlach C, Mecucci C, Schnittger S, Kohlmann A, Mancini M, Cuneo A, Testoni N, Rege-Cambrin G, Santucci A, Vignetti M, Fazi P, Martelli MP, Haferlach T, Falini B,. AML with mutated NPM1 carrying a normal or aberrant karyotype show overlapping biologic, pathologic, immunophenotypic, and prognostic features. Blood 2009; 114: 3024-3032.
51. Dvorakova D, Racil Z, Jeziskova I, Palasek I, Protivankova M, Lengerova M, Razga F, Mayer J,. Monitoring of minimal residual disease in acute myeloid leukemia with frequent and rare patient-specific NPM1 mutations. Am J Hematol 2010; 85: 926-929.
52. 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.
53. Wang ES, Sait SNJ, Gold D, Mashtare T, Starostik P, Ford LA, Wetzler M, Nowak NJ, Deeb G,. Genomic, immunophenotypic, and NPM1/FLT3 mutational studies on 17 patients with normal karyotype acute myeloid leukemia (AML) followed by aberrant karyotype AML at relapse. Cancer Genet Cytogenet 2010; 202: 101-107.
54. Bachas C, Schuurhuis GJ, Assaraf YG, Kwidama ZJ, Kelder A, Wouters F, Snel a N, Kaspers GJL, Cloos J,. The role of minor subpopulations within the leukemic blast compartment of AML patients at initial diagnosis in the development of relapse. Leukemia 2012; 26: 1313-1320.
55. Falini B, Martelli MP, Bolli N, Sportoletti P, Liso A, Tiacci E, Haferlach T,. Acute myeloid leukemia with mutated nucleophosmin (NPM1): is it a distinct entity? Blood 2011; 117: 1109-1120.
56. Arber, Md D a., Stein, Md AS, Carter, Ms NH, Ikle, PhD D, Forman, Md SJ, Slovak ML, Forman SJ,. Prognostic impact of acute myeloid leukemia classification: importance of detection of recurring cytogenetic abnormalities and multilineage dysplasia on survival. Am J Clin Pathol 2003; 119: 672-680.
57. Cheng Y, Wang Y, Wang H, Chen Z, Lou J, Xu H, Qian W, Meng H, Lin M, Jin J,. Cytogenetic profile of de novo acute myeloid leukemia: A study based on 1432 patients in a single institution of China. Leukemia 2009; 23: 1801-1806.
58. Grimwade D, Hills RK, Moorman A V, Walker H, Chatters S, Goldstone AH, Wheatley K, Harrison CJ, Burnett AK,. Refinement of cytogenetic classification in acute myeloid leukemia: determination of prognostic significance of rare recurring chromosomal abnormalities among 5876 younger adult patients treated in the United Kingdom Medical Research Council trials. Blood 2010; 116: 354-365.
59. Khoury H, Dalal BI, Nevill TJ, Horsman DE, Barnett MJ, Shepherd JD, Toze CL, Conneally EA, Sutherland HJ, Hogge DE, Nantel SH,. Acute myelogenous leukemia with t(8;21)-identification of a specific immunophenotype. Leuk Lymphoma 2003; 44: 1713-1718.
60. Khoury H, Dalal BI, Nantel SH, Horsman DE, Lavoie JC, Shepherd JD, Hogge DE, Toze CL, Song KW, Forrest DL, Sutherland HJ, Nevill TJ,. Correlation between karyotype and quantitative immunophenotype in acute myelogenous leukemia with t(8;21). Mod Pathol 2004; 17: 1211-1216.
61. Zheng J, Wang X, Hu Y, Yang J, Liu J, He Y, Gong Q, Yao J, Li X, Du W, Huang S,. A correlation study of immunophenotypic, cytogenetic, and clinical features of 180 AML patients in China. Cytometry B Clin Cytom 2008; 74B: 25-29.
62. Baer MR, Stewart CC, Lawrence D, Arthur DC, Byrd JC, Davey FR, Schiffer CA, Bloomfield CD,. Expression of the neural cell adhesion molecule CD56 is associated with short remission duration and survival in acute myeloid leukemia with t(8;21)(q22;q22). Blood 1997; 90: 1643-1648.
63. Claxton DF, Liu P, Hsu HB, Marlton P, Hester J, Collins F, Deisseroth a B, Rowley JD, Siciliano MJ,. Detection of fusion transcripts generated by the inversion 16 chromosome in acute myelogenous leukemia. Blood 1994; 83: 1750-1756.
64. Paietta E, Wiernik PH, Andersen J, Bennett J, Yunis J,. Acute myeloid leukemia M4 with inv(16) (p13q22) exhibits a specific immunophenotype with CD2 expression [letter]. Blood 1993; 82: 2595-2596.
65. Adriaansen HJ, te Boekhorst PA, Hagemeijer AM, van der Schoot CE, Delwel HR, van Dongen JJ,. Acute myeloid leukemia M4 with bone marrow eosinophilia (M4Eo) and inv(16)(p13q22) exhibits a specific immunophenotype with CD2 expression. Blood 1993; 81: 3043-3051.
66. Dunphy CH,. Comprehensive review of adult acute myelogenous leukemia: cytomorphological, enzyme cytochemical, flow cytometric immunophenotypic, and cytogenetic findings. J Clin Lab Anal 1999; 13: 19-26.
67. Medeiros BC, Kohrt HE, Arber DA, Bangs CD, Cherry AM, Majeti R, Kogel KE, Azar CA, Patel S, Alizadeh AA,. Immunophenotypic features of acute myeloid leukemia with inv(3)(q21q26.2)/t(3;3)(q21;q26.2). Leuk Res 2010; 34: 594-597.
68. Paietta E,. Expression of cell-surface antigens in acute promyelocytic leukaemia. Best Pract Res Clin Haematol 2003; 16: 369-385.
69. Paietta E, Goloubeva O, Neuberg D, Bennett JM, Gallagher R, Racevskis J, Dewald G, Wiernik PH, Tallman MS,. A surrogate marker profile for PML/RAR alpha expressing acute promyelocytic leukemia and the association of immunophenotypic markers with morphologic and molecular subtypes. Cytometry B Clin Cytom 2004; 59B: 1-9.
70. Orfao A, Chillon MC, Bortoluci AM, Lopez-Berges MC, Garcia-Sanz R, Gonzalez M, Tabernero MD, Garcia-Marcos MA, Rasillo AI, Hernandez-Rivas J, San Miguel JF,. The flow cytometric pattern of CD34, CD15 and CD13 expression in acute myeloblastic leukemia is highly characteristic of the presence of PML-RARa gene rearrangements. Haematologica 1999; 84: 405-412.
71. Guglielmi C, Martelli MP, Diverio D, Fenu S, Vegna ML, Cantù-Rajnoldi A, Biondi A, Cocito MG, Del Vecchio L, Tabilio A, Avvisati G, Basso G, Lo Coco F,. Immunophenotype of adult and childhood acute promyelocytic leukaemia: Correlation with morphology, type of PML gene breakpoint and clinical outcome. A cooperative Italian study on 196 cases. Br J Haematol 1998; 102: 1035-1041.
72. Small D,. FLT3 mutations: biology and treatment. Hematology Am Soc Hematol Educ Program 2006: 178-184.
73. Wagner K, Damm F, Thol F, Göhring G, Görlich K, Heuser M, Schäfer I, Schlegelberger B, Heil G, Ganser A, Krauter J,. FLT3-internal tandem duplication and age are the major prognostic factors in patients with relapsed acute myeloid leukemia with normal karyotype. Haematologica 2011; 96: 681-686.
74. Chauhan PS, Bhushan B, Mishra AK, Singh LC, Saluja S, Verma S, Gupta DK, Mittal V, Chaudhry S, Kapur S,. Mutation of FLT3 gene in acute myeloid leukemia with normal cytogenetics and its association with clinical and immunophenotypic features. Med Oncol 2011; 28: 544-551.
75. Munoz L, Aventin A, Villamor N, Junca J, Acebedo G, Domingo A, Rozman M, Torres JP, Tormo M, Nomdedeu JF,. Immunophenotypic findings in acute myeloid leukemia with FLT3 internal tandem duplication. Haematologica 2003; 88: 637-645.
76. Hoehn D, Medeiros LJ, Chen SS, Tian T, Jorgensen JL, Ahmed Y, Lin P,. CD117 expression is a sensitive but nonspecific predictor of FLT3 mutation in T acute lymphoblastic leukemia and T/myeloid acute leukemia. Am J Clin Pathol 2012; 137: 213-219.
77. Falini B, Mecucci C, Tiacci E, Alcalay M, Rosati R, Pasqualucci L, La Starza R, Diverio D, Colombo E, Santucci A, Bigerna B, Pacini R, Pucciarini A, Liso A, Vignetti M, Fazi P, Meani N, Pettirossi V, Saglio G, Mandelli F, Lo-Coco F, Pelicci P-G, Martelli MF,. Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N Engl J Med 2005; 352: 254-266.
78. De Propris MS, Raponi S, Diverio D, Milani ML, Meloni G, Falini B, Foà R, Guarini A,. High CD33 expression levels in acute myeloid leukemia cells carrying the nucleophosmin (NPM1) mutation. Haematologica 2011; 96: 1548-1551.
79. Tsykunova G, Reikvam H, Hovland R, Bruserud Ø,. The surface molecule signature of primary human acute myeloid leukemia (AML) cells is highly associated with NPM1 mutation status. Leukemia 2012; 26: 557-559.
80. Nomdedeu J, Bussaglia E, Villamor N, Martinez C, Esteve J, Tormo M, Estivill C, Queipo MP, Guardia R, Carricondo M, Hoyos M, Llorente A, Juncà J, Gallart M, Domingo A, Bargay J, Mascarõ M, Moraleda JM, Florensa L, Ribera JM, Gallardo D, Brunet S, Aventin A, Sierra J,. Immunophenotype of acute myeloid leukemia with NPM mutations: prognostic impact of the leukemic compartment size. Leuk Res 2011; 35: 163-168.
81. Kern W, Haferlach C, Bacher U, Haferlach T, Schnittger S,. Flow cytometric identification of acute myeloid leukemia with limited differentiation and NPM1 type A mutation: A new biologically defined entity. Leukemia 2009; 23: 1361-1364.
82. Oelschlaegel U, Mohr B, Schaich M, Kroschinsky F, Parmentier S, Bornhäuser M, Ehninger G, Thiede C,. Reply to: "Flow cytometric identification of acute myeloid leukemia with limited differentiation and NPM1 type A mutation: a new biologically defined entity" by Kern et al. Leukemia 2011; 25: 895-897.
83. Nerlov C,. C/EBPalpha mutations in acute myeloid leukaemias. Nat Rev Cancer 2004; 4: 394-400.
84. Schlenk RF, Döhner K, Krauter J, Fröhling S, Corbacioglu A, Bullinger L, Habdank M, Späth D, Morgan M, Benner A, Schlegelberger B, Heil G, Ganser A, Döhner H,. Mutations and treatment outcome in cytogenetically normal acute myeloid leukemia. N Engl J Med 2008; 358: 1909-1918.
85. Lin L-I, Chen C-Y, Lin D-T, Tsay W, Tang J-L, Yeh Y-C, Shen H-L, Su F-H, Yao M, Huang S-Y, Tien H-F,. Characterization of CEBPA mutations in acute myeloid leukemia: most patients with CEBPA mutations have biallelic mutations and show a distinct immunophenotype of the leukemic cells. Clin Cancer Res 2005; 11: 1372-1379.
86. Ottone T, Zaza S, Divona M, Hasan SK, Lavorgna S, Laterza S, Cicconi L, Panetta P, Giandomenico J Di, Cittadini M, Ciardi C, Montefusco E, Franchi A, Annino L, Venditti A, Amadori S, Lo-Coco F,. Identification of emerging FLT3 ITD-positive clones during clinical remission and kinetics of disease relapse in acute myeloid leukaemia with mutated nucleophosmin. Br J Haematol 2013; 161: 533-540.
87. Costello RT, Mallet F, Gaugler B, Sainty D, Arnoulet C, Gastaut JA, Olive D,. Human acute myeloid leukemia CD34+/CD38- progenitor cells have decreased sensitivity to chemotherapy and Fas-induced apoptosis, reduced immunogenicity, and impaired dendritic cell transformation capacities. Cancer Res 2000; 60: 4403-4411.
88. Terwijn M, Rutten AP, Kelder A, Snel AN, Scholten WJ, Zweegman S, Ossenkoppele GJ, Schuurhuis GJ,. Accurate detection of residual leukemic stem cells in remission bone marrow predicts relapse in acute myeloid leukemia patients. ASH Annual Meeting Abstracts 2010; 116: 759.
89. Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC, Welch JS, Ritchey JK, Young MA, Lamprecht T, McLellan MD, McMichael JF, Wallis JW, Lu C, Shen D, Harris CC, Dooling DJ, Fulton RS, Fulton LL, Schmidt H, Kalicki-Veizer J, Magrini VJ, Cook L, McGrath SD, Vickery TL, Wendl MC, Heath S, Watson MA, Link DC, Tomasson MH, Shannon WD, Payton JE, Kulkarni S, Westervelt P, Walter MJ, Graubert TA, Mardis ER, Wilson RK, DiPersio JF,. Clonal evolution in relapsed acute myeloid leukemia revealed by whole genome sequencing. Nature 2012; 481: 506-510.
90. Valent P, Bonnet D, De Maria R, Lapidot T, Copland M, Melo J V, Chomienne C, Ishikawa F, Schuringa JJ, Stassi G, Huntly B, Herrmann H, Soulier J, Roesch A, Schuurhuis GJ, Wöhrer S, Arock M, Zuber J, Cerny-Reiterer S, Johnsen HE, Andreeff M, Eaves C,. Cancer stem cell definitions and terminology: The devil is in the details. Nat Rev Cancer 2012; 12: 767-775.
91. Rausei-Mills V, Chang KL, Gaal KK, Weiss LM, Huang Q,. Aberrant expression of CD7 in myeloblasts is highly associated with de novo acute myeloid leukemias with FLT3/ITD mutation. Am J Clin Pathol 2008; 129: 624-629.
92. Pandolfi A, Barreyro L, Steidl U,. Concise review: Preleukemic stem cells: molecular biology and clinical implications of the precursors to leukemia stem cells. Stem Cells Transl Med 2013; 2: 143-150.
93. Mullighan CG, Phillips LA, Su X, Ma J, Miller CB, Shurtleff SA, Downing JR,. Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science (New York, N.Y.) 2008; 322: 1377-1380.