Combining gene mutation with gene expression analysis improves outcome prediction in acute promyelocytic leukemia

Blood - Tập 134 - Trang 951-959 - 2019
Antonio R. Lucena-Araujo1,2,3, Juan L. Coelho-Silva1,2,3, Diego A. Pereira-Martins1,2,3, Douglas R. Silveira4, Luisa C. Koury2, Raul A.M. Melo5, Rosane Bittencourt6, Katia Pagnano7, Ricardo Pasquini8, Elenaide C. Nunes8, Evandro M. Fagundes9, Ana B. Gloria9, Fábio Kerbauy10, Maria de Lourdes Chauffaille10, Israel Bendit4, Vanderson Rocha3,4,11, Armand Keating12, Martin S. Tallman13, Raul C. Ribeiro14, Richard Dillon15
1Department of Genetics, Federal University of Pernambuco, Recife, Brazil
2Department of Internal Medicine, Medical School of Ribeirao Preto, Ribeirao Preto, Brazil
3Center for Cell Based Therapy, University of Sao Paulo, Ribeirao Preto, Brazil
4Hematology Division, Faculdade de Medicina, University of Sao Paulo, Sao Paulo, Brazil
5Department of Internal Medicine, University of Pernambuco, Recife, Brazil
6Hematology Division, Federal University of Rio Grande do Sul, Porto Alegre, Brazil;
7Hematology and Hemotherapy Center, University of Campinas, Campinas, Brazil
8Hematology Division, Federal University of Parana, Curitiba, Brazil
9Hematology Division, Federal University of Minas Gerais, Belo Horizonte, Brazil
10Department of Hematology, Federal University of Sao Paulo, Sao Paulo, Brazil
11Department of Haematology, Churchill Hospital, Oxford University, Oxford, United Kingdom
12Princess Margaret Cancer Centre, Toronto, ON, Canada
13Leukemia Service, Memorial Sloan Kettering Cancer Center, New York, NY;
14Department of Oncology, St. Jude Children's Research Hospital, Memphis, TN
15Department of Medical and Molecular Genetics, Faculty of Life Sciences and Medicine, King's College London, London, United Kingdom

Tóm tắt

Abstract Luceno-Araujo et al use assays of mutations associated with myeloid malignancy to propose an integrative prognostic score for acute promyelocytic leukemia (ISAPL) in patients treated with all-trans retinoic acid and anthracycline-based therapy. They demonstrate that the ISAPL is superior for predicting outcomes and identifying patients who may benefit from alternative therapies to maximize their chance of a cure.

Tài liệu tham khảo

Jácomo, 2007, Clinical features and outcomes of 134 Brazilians with acute promyelocytic leukemia who received ATRA and anthracyclines, Haematologica, 92, 1431, 10.3324/haematol.10874 Lehmann, 2011, Continuing high early death rate in acute promyelocytic leukemia: a population-based report from the Swedish Adult Acute Leukemia Registry, Leukemia, 25, 1128, 10.1038/leu.2011.78 Park, 2011, Early death rate in acute promyelocytic leukemia remains high despite all-trans retinoic acid, Blood, 118, 1248, 10.1182/blood-2011-04-346437 Rego, 2013, Improving acute promyelocytic leukemia (APL) outcome in developing countries through networking, results of the International Consortium on APL, Blood, 121, 1935, 10.1182/blood-2012-08-449918 Sanz, 2015, All-trans retinoic acid with daunorubicin or idarubicin for risk-adapted treatment of acute promyelocytic leukaemia: a matched-pair analysis of the PETHEMA LPA-2005 and IC-APL studies, Ann Hematol, 94, 1347, 10.1007/s00277-015-2393-0 Sanz, 2000, Definition of relapse risk and role of nonanthracycline drugs for consolidation in patients with acute promyelocytic leukemia: a joint study of the PETHEMA and GIMEMA cooperative groups, Blood, 96, 1247 Lo-Coco, 2013, Retinoic acid and arsenic trioxide for acute promyelocytic leukemia, N Engl J Med, 369, 111, 10.1056/NEJMoa1300874 Platzbecker, 2017, Improved outcomes with retinoic acid and arsenic trioxide compared with retinoic acid and chemotherapy in non-high-risk acute promyelocytic leukemia: final results of the randomized Italian-German APL0406 trial, J Clin Oncol, 35, 605, 10.1200/JCO.2016.67.1982 Abaza, 2017, Long-term outcome of acute promyelocytic leukemia treated with all-trans-retinoic acid, arsenic trioxide, and gemtuzumab, Blood, 129, 1275, 10.1182/blood-2016-09-736686 Lucena-Araujo, 2015, High ΔNp73/TAp73 ratio is associated with poor prognosis in acute promyelocytic leukemia, Blood, 126, 2302, 10.1182/blood-2015-01-623330 Lucena-Araujo, 2014, Prognostic impact of KMT2E transcript levels on outcome of patients with acute promyelocytic leukaemia treated with all-trans retinoic acid and anthracycline-based chemotherapy: an International Consortium on Acute Promyelocytic Leukaemia study, Br J Haematol, 166, 540, 10.1111/bjh.12921 Lucena-Araujo, 2014, Internal tandem duplication of the FLT3 gene confers poor overall survival in patients with acute promyelocytic leukemia treated with all-trans retinoic acid and anthracycline-based chemotherapy: an International Consortium on Acute Promyelocytic Leukemia study, Ann Hematol, 93, 2001, 10.1007/s00277-014-2142-9 Sunter, 2012, A functional variant in the core promoter of the CD95 cell death receptor gene predicts prognosis in acute promyelocytic leukemia, Blood, 119, 196, 10.1182/blood-2011-04-349803 Montesinos, 2011, Clinical significance of CD56 expression in patients with acute promyelocytic leukemia treated with all-trans retinoic acid and anthracycline-based regimens, Blood, 117, 1799, 10.1182/blood-2010-04-277434 Ferrara, 2000, CD56 expression is an indicator of poor clinical outcome in patients with acute promyelocytic leukemia treated with simultaneous all-trans-retinoic acid and chemotherapy, J Clin Oncol, 18, 1295, 10.1200/JCO.2000.18.6.1295 Lucena-Araujo, 2017, Clinical impact of BAALC expression in high-risk acute promyelocytic leukemia, Blood Adv, 1, 1807, 10.1182/bloodadvances.2017005926 Damm, 2011, Prognostic importance of histone methyltransferase MLL5 expression in acute myeloid leukemia, J Clin Oncol, 29, 682, 10.1200/JCO.2010.31.1118 Tang, 2009, High Id1 expression is associated with poor prognosis in 237 patients with acute myeloid leukemia, Blood, 114, 2993, 10.1182/blood-2009-05-223115 Kapelko-Slowik, 2016, Elevated PIM2 gene expression is associated with poor survival of patients with acute myeloid leukemia, Leuk Lymphoma, 57, 2140, 10.3109/10428194.2015.1124991 Santamaría, 2009, Molecular stratification model for prognosis in cytogenetically normal acute myeloid leukemia, Blood, 114, 148, 10.1182/blood-2008-11-187724 Marcucci, 2005, 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, 23, 9234, 10.1200/JCO.2005.03.6137 Barragán, 2004, Prognostic implications of Wilms’ tumor gene (WT1) expression in patients with de novo acute myeloid leukemia, Haematologica, 89, 926 van Dongen, 1999, Standardized RT-PCR analysis of fusion gene transcripts from chromosome aberrations in acute leukemia for detection of minimal residual disease. Report of the BIOMED-1 Concerted Action: investigation of minimal residual disease in acute leukemia, Leukemia, 13, 1901, 10.1038/sj.leu.2401592 Kiyoi, 1999, Prognostic implication of FLT3 and N-RAS gene mutations in acute myeloid leukemia, Blood, 93, 3074 Stone, 2017, Midostaurin plus chemotherapy for acute myeloid leukemia with a FLT3 mutation, N Engl J Med, 377, 454, 10.1056/NEJMoa1614359 Döhner, 2017, Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel, Blood, 129, 424, 10.1182/blood-2016-08-733196 Heagerty, 2005, Survival model predictive accuracy and ROC curves, Biometrics, 61, 92, 10.1111/j.0006-341X.2005.030814.x Harrell, 1982, Evaluating the yield of medical tests, JAMA, 247, 2543, 10.1001/jama.1982.03320430047030 Benicio, 2017, Evaluation of the European LeukemiaNet recommendations for predicting outcomes of patients with acute myeloid leukemia treated in low- and middle-income countries (LMIC): A Brazilian experience, Leuk Res, 60, 109, 10.1016/j.leukres.2017.07.005 Davison, 1997, Bootstrap Methods and Their Application, 10.1017/CBO9780511802843 Harrell, 1998, Development of a clinical prediction model for an ordinal outcome: the World Health Organization Multicentre Study of Clinical Signs and Etiological agents of Pneumonia, Sepsis and Meningitis in Young Infants, Stat Med, 17, 909, 10.1002/(SICI)1097-0258(19980430)17:8<909::AID-SIM753>3.0.CO;2-O Harrell, 1996, Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors, Stat Med, 15, 361, 10.1002/(SICI)1097-0258(19960229)15:4<361::AID-SIM168>3.0.CO;2-4 Damm, 2011, Integrative prognostic risk score in acute myeloid leukemia with normal karyotype, Blood, 117, 4561, 10.1182/blood-2010-08-303479 Hecht, 2015, Prognostic importance of expression of the Wilms’ tumor 1 gene in newly diagnosed acute promyelocytic leukemia, Leuk Lymphoma, 56, 2289, 10.3109/10428194.2014.990011 Nolte, 2013, In acute promyelocytic leukemia (APL) low BAALC gene expression identifies a patient group with favorable overall survival and improved relapse free survival, Leuk Res, 37, 378, 10.1016/j.leukres.2012.11.018 Barragán, 2011, Prognostic value of FLT3 mutations in patients with acute promyelocytic leukemia treated with all-trans retinoic acid and anthracycline monochemotherapy, Haematologica, 96, 1470, 10.3324/haematol.2011.044933 Hecht, 2013, High expression of the Ets-related gene (ERG) is an independent prognostic marker for relapse-free survival in patients with acute promyelocytic leukemia [published correction appears in Ann Hematol. 2014;93(8):1447], Ann Hematol, 92, 443, 10.1007/s00277-012-1648-2 Grossmann, 2012, A novel hierarchical prognostic model of AML solely based on molecular mutations, Blood, 120, 2963, 10.1182/blood-2012-03-419622 Patel, 2012, Prognostic relevance of integrated genetic profiling in acute myeloid leukemia, N Engl J Med, 366, 1079, 10.1056/NEJMoa1112304 Pastore, 2014, Combined molecular and clinical prognostic index for relapse and survival in cytogenetically normal acute myeloid leukemia, J Clin Oncol, 32, 1586, 10.1200/JCO.2013.52.3480 Thol, 2012, Prognostic significance of combined MN1, ERG, BAALC, and EVI1 (MEBE) expression in patients with myelodysplastic syndromes, Ann Hematol, 91, 1221, 10.1007/s00277-012-1457-7 Hecht, 2015, A molecular risk score integrating BAALC, ERG and WT1 expression levels for risk stratification in acute promyelocytic leukemia, Leuk Res, 39, 1172, 10.1016/j.leukres.2015.08.010 Hecht, 2017, Validation of a molecular risk score for prognosis of patients with acute promyelocytic leukemia treated with all-trans retinoic acid and chemotherapy-containing regimens, Clin Lymphoma Myeloma Leuk, 17, 889, 10.1016/j.clml.2017.08.095 Brand, 2013, A standardized microarray assay for the independent gene expression markers in AML: EVI1 and BAALC, Exp Hematol Oncol, 2, 7, 10.1186/2162-3619-2-7 Lucena-Araujo, 2017, ΔNp73 overexpression promotes resistance to apoptosis but does not cooperate with PML/RARA in the induction of an APL-leukemic phenotype, Oncotarget, 8, 8475, 10.18632/oncotarget.14295 Kelly, 2002, PML/RARalpha and FLT3-ITD induce an APL-like disease in a mouse model, Proc Natl Acad Sci USA, 99, 8283, 10.1073/pnas.122233699 Agrawal-Singh, 2010, Pim2 cooperates with PML-RARalpha to induce acute myeloid leukemia in a bone marrow transplantation model, Blood, 115, 4507, 10.1182/blood-2009-03-210070 Heuser, 2012, Functional role of BAALC in leukemogenesis, Leukemia, 26, 532, 10.1038/leu.2011.228 Esnault, 2019, FLT3-ITD impedes retinoic acid, but not arsenic, responses in murine acute promyelocytic leukemias, Blood, 133, 1495, 10.1182/blood-2018-07-866095