Skip to main content
Erschienen in: Annals of Hematology 11/2019

06.09.2019 | Original Article

The prognostic significance of Wilms’ tumor gene 1 (WT1) expression at diagnosis in adults with Ph-negative B cell precursor acute lymphoblastic leukemia

verfasst von: Ya-Zhen Qin, Qian Jiang, Lan-Ping Xu, Hao Jiang, Yu Wang, Xiao-Su Zhao, Zong-Ru Li, Yue-Yun Lai, Yan-Rong Liu, Xiao-Hui Zhang, Kai-Yan Liu, Xiao-Jun Huang

Erschienen in: Annals of Hematology | Ausgabe 11/2019

Einloggen, um Zugang zu erhalten

Abstract

The prognostic significance of Wilms’ tumor gene 1 (WT1) expression at diagnosis in adults with B cell precursor acute lymphoblastic leukemia (BCP-ALL) remains poorly understood. A total of 257 adults with Ph-negative BCP-ALL who were consecutively diagnosed and received at least 1 course of induction therapy at our institute were retrospectively analyzed. The WT1 expression patterns were significantly different among the molecularly and cytogenetically defined groups (E2A-PBX1, TEL-AML1, and MLL rearrangements; high hyperdiploidy and B-other). By considering the WT1 expression pattern and the relapse status, 2 cutoff values, 1.8% and 7.2%, were arbitrarily selected to place patients into WT1-low, WT1-inter, and WT1-high groups. In the B-other patients who achieved complete remission (CR), WT1-low and WT1-high patients had similar 3-year relapse-free survival (RFS), disease-free survival (DFS), and overall survival (OS) rates, which were all significantly lower than those of WT1-inter patients. The combined WT1-low/high expression group (n = 132) had significantly lower 3-year RFS, DFS, and OS rates compared with the WT1-inter group (n = 63) of B-other patients (RFS and DFS all P < 0.0001; OS P = 0.0018 and 0.0008). WT1 low/high expression as well as treating with chemotherapy only was independent poor prognostic factors for RFS, DFS, and OS in the B-other patients who achieved CR. Therefore, the molecularly and cytogenetically defined adult Ph-negative BCP-ALL groups have characteristic WT1 expression patterns, and WT1 low/high expression at diagnosis predicts poor outcome in B-other patients.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Thomas DA, O’Brien S, Faderl S, Garcia-Manero G, Ferrajoli A, Wierda W, Ravandi F, Verstovsek S, Jorgensen JL, Bueso-Ramos C, Andreeff M, Pierce S, Garris R, Keating MJ, Cortes J, Kantarjian HM (2010) Chemoimmunotherapy with a modified hyper-CVAD and rituximab regimen improves outcome in de novo Philadelphia chromosome-negative precursor B-lineage acute lymphoblastic leukemia. J Clin Oncol 28(24):3880–3889CrossRef Thomas DA, O’Brien S, Faderl S, Garcia-Manero G, Ferrajoli A, Wierda W, Ravandi F, Verstovsek S, Jorgensen JL, Bueso-Ramos C, Andreeff M, Pierce S, Garris R, Keating MJ, Cortes J, Kantarjian HM (2010) Chemoimmunotherapy with a modified hyper-CVAD and rituximab regimen improves outcome in de novo Philadelphia chromosome-negative precursor B-lineage acute lymphoblastic leukemia. J Clin Oncol 28(24):3880–3889CrossRef
2.
Zurück zum Zitat Ribera JM, Oriol A, Morgades M, Montesinos P, Sarrà J, González-Campos J, Brunet S, Tormo M, Fernández-Abellán P, Guàrdia R, Bernal MT, Esteve J, Barba P, Moreno MJ, Bermúdez A, Cladera A, Escoda L, García-Boyero R, Del Potro E, Bergua J, Amigo ML, Grande C, Rabuñal MJ, Hernández-Rivas JM, Feliu E (2014) Treatment of high-risk Philadelphia chromosome-negative acute lymphoblastic leukemia in adolescents and adults according to early cytologic response and minimal residual disease after consolidation assessed by flow cytometry: final results of the PETHEMA ALL-AR-03 trial. J Clin Oncol 32(15):1595–1604CrossRef Ribera JM, Oriol A, Morgades M, Montesinos P, Sarrà J, González-Campos J, Brunet S, Tormo M, Fernández-Abellán P, Guàrdia R, Bernal MT, Esteve J, Barba P, Moreno MJ, Bermúdez A, Cladera A, Escoda L, García-Boyero R, Del Potro E, Bergua J, Amigo ML, Grande C, Rabuñal MJ, Hernández-Rivas JM, Feliu E (2014) Treatment of high-risk Philadelphia chromosome-negative acute lymphoblastic leukemia in adolescents and adults according to early cytologic response and minimal residual disease after consolidation assessed by flow cytometry: final results of the PETHEMA ALL-AR-03 trial. J Clin Oncol 32(15):1595–1604CrossRef
3.
Zurück zum Zitat Ogawa H, Tamaki H, Ikegame K, Soma T, Kawakami M, Tsuboi A, Kim EH, Hosen N, Murakami M, Fujioka T, Masuda T, Taniguchi Y, Nishida S, Oji Y, Oka Y, Sugiyama H (2003) The usefulness of monitoring WT1 gene transcripts for the prediction and management of relapse following allogeneic stem cell transplantation in acute type leukemia. Blood 101(5):1698–1704CrossRef Ogawa H, Tamaki H, Ikegame K, Soma T, Kawakami M, Tsuboi A, Kim EH, Hosen N, Murakami M, Fujioka T, Masuda T, Taniguchi Y, Nishida S, Oji Y, Oka Y, Sugiyama H (2003) The usefulness of monitoring WT1 gene transcripts for the prediction and management of relapse following allogeneic stem cell transplantation in acute type leukemia. Blood 101(5):1698–1704CrossRef
4.
Zurück zum Zitat Cilloni D, Renneville A, Hermitte F, Hills RK, Daly S, Jovanovic JV, Gottardi E, Fava M, Schnittger S, Weiss T, Izzo B, Nomdedeu J, van der Heijden A, van der Reijden BA, Jansen JH, van der Velden VH, Ommen H, Preudhomme C, Saglio G, Grimwade D (2009) 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 27(31):5195–5201CrossRef Cilloni D, Renneville A, Hermitte F, Hills RK, Daly S, Jovanovic JV, Gottardi E, Fava M, Schnittger S, Weiss T, Izzo B, Nomdedeu J, van der Heijden A, van der Reijden BA, Jansen JH, van der Velden VH, Ommen H, Preudhomme C, Saglio G, Grimwade D (2009) 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 27(31):5195–5201CrossRef
5.
Zurück zum Zitat Nomdedéu JF, Esquirol A, Carricondo M, Pratcorona M, Hoyos M, Garrido A, Rubio M, Bussaglia E, García-Cadenas I, Estivill C, Brunet S, Martino R, Sierra J (2018) Bone marrow WT1 levels in allogeneic hematopoietic stem cell transplantation for acute myelogenous leukemia and myelodysplasia: clinically relevant time points and 100 copies threshold value. Biol Blood Marrow Transplant 24(1):55–63CrossRef Nomdedéu JF, Esquirol A, Carricondo M, Pratcorona M, Hoyos M, Garrido A, Rubio M, Bussaglia E, García-Cadenas I, Estivill C, Brunet S, Martino R, Sierra J (2018) Bone marrow WT1 levels in allogeneic hematopoietic stem cell transplantation for acute myelogenous leukemia and myelodysplasia: clinically relevant time points and 100 copies threshold value. Biol Blood Marrow Transplant 24(1):55–63CrossRef
6.
Zurück zum Zitat Nomdedéu JF, Hoyos M, Carricondo M, Bussaglia E, Estivill C, Esteve J, Tormo M, Duarte R, Salamero O, de Llano MP, García A, Bargay J, Heras I, Martí-Tutusaus JM, Llorente A, Ribera JM, Gallardo D, Aventin A, Brunet S, Sierra J, CETLAM Group (2013) Bone marrow WT1 levels at diagnosis, post-induction and post-intensification in adult de novo AML. Leukemia 27(11):2157–2164CrossRef Nomdedéu JF, Hoyos M, Carricondo M, Bussaglia E, Estivill C, Esteve J, Tormo M, Duarte R, Salamero O, de Llano MP, García A, Bargay J, Heras I, Martí-Tutusaus JM, Llorente A, Ribera JM, Gallardo D, Aventin A, Brunet S, Sierra J, CETLAM Group (2013) Bone marrow WT1 levels at diagnosis, post-induction and post-intensification in adult de novo AML. Leukemia 27(11):2157–2164CrossRef
7.
Zurück zum Zitat Yi-Ning Y, Xiao-rui W, Chu-xian Z, Chun W, You-wen Q (2015) Prognostic significance of diagnosed WT1 level in acute myeloid leukemia: a meta-analysis. Ann Hematol 94(6):929–938CrossRef Yi-Ning Y, Xiao-rui W, Chu-xian Z, Chun W, You-wen Q (2015) Prognostic significance of diagnosed WT1 level in acute myeloid leukemia: a meta-analysis. Ann Hematol 94(6):929–938CrossRef
8.
Zurück zum Zitat Chiusa L, Francia di Celle P, Campisi P, Ceretto C, Marmont F, Pich A (2006) Prognostic value of quantitative analysis of WT1 gene transcripts in adult acute lymphoblastic leukemia. Haematologica 91(2):270–271PubMed Chiusa L, Francia di Celle P, Campisi P, Ceretto C, Marmont F, Pich A (2006) Prognostic value of quantitative analysis of WT1 gene transcripts in adult acute lymphoblastic leukemia. Haematologica 91(2):270–271PubMed
9.
Zurück zum Zitat Busse A, Gökbuget N, Siehl JM, Hoelzer D, Schwartz S, Rietz A, Thiel E, Keilholz U (2009) Wilms’ tumor gene 1 (WT1) expression in subtypes of acute lymphoblastic leukemia (ALL) of adults and impact on clinical outcome. Ann Hematol 88(12):1199–1205CrossRef Busse A, Gökbuget N, Siehl JM, Hoelzer D, Schwartz S, Rietz A, Thiel E, Keilholz U (2009) Wilms’ tumor gene 1 (WT1) expression in subtypes of acute lymphoblastic leukemia (ALL) of adults and impact on clinical outcome. Ann Hematol 88(12):1199–1205CrossRef
10.
Zurück zum Zitat Yang S, Wang J, Zhao T, Jia J, Zhu H, Jiang H, Lu J, Jiang B, Shi H, Liu Y, Lai Y, Xu L, Huang X, Jiang Q (2017) CD20 expression sub-stratifies standard-risk patients with B cell precursor acute lymphoblastic leukemia. Oncotarget 8(62):105397–105406PubMedPubMedCentral Yang S, Wang J, Zhao T, Jia J, Zhu H, Jiang H, Lu J, Jiang B, Shi H, Liu Y, Lai Y, Xu L, Huang X, Jiang Q (2017) CD20 expression sub-stratifies standard-risk patients with B cell precursor acute lymphoblastic leukemia. Oncotarget 8(62):105397–105406PubMedPubMedCentral
11.
Zurück zum Zitat Yan CH, Liu DH, Liu KY, Xu LP, Liu YR, Chen H, Han W, Wang Y, Qin YZ, Huang XJ (2012) Risk stratification-directed donor lymphocyte infusion could reduce relapse of standard-risk acute leukemia patients after allogeneic hematopoietic stem cell transplantation. Blood 119(14):3256–3262CrossRef Yan CH, Liu DH, Liu KY, Xu LP, Liu YR, Chen H, Han W, Wang Y, Qin YZ, Huang XJ (2012) Risk stratification-directed donor lymphocyte infusion could reduce relapse of standard-risk acute leukemia patients after allogeneic hematopoietic stem cell transplantation. Blood 119(14):3256–3262CrossRef
12.
Zurück zum Zitat Qin Y, Zhu H, Jiang B, Li J, Lu X, Li L, Ruan G, Liu Y, Chen S, Huang X (2009) Expression patterns of WT1 and PRAME in acute myeloid leukemia patients and their usefulness for monitoring minimal residual disease. Leuk Res 33(3):384–390CrossRef Qin Y, Zhu H, Jiang B, Li J, Lu X, Li L, Ruan G, Liu Y, Chen S, Huang X (2009) Expression patterns of WT1 and PRAME in acute myeloid leukemia patients and their usefulness for monitoring minimal residual disease. Leuk Res 33(3):384–390CrossRef
13.
Zurück zum Zitat Qin YZ, Zhu HH, Liu YR, Wang YZ, Shi HX, Lai YY, Xu LP, Liu DH, Jiang Q, Li LD, Jiang B, Liu KY, Huang XJ (2013) PRAME and WT1 transcripts constitute a good molecular marker combination for monitoring minimal residual disease in myelodysplastic syndromes. Leuk Lymphoma 54(7):1442–1449CrossRef Qin YZ, Zhu HH, Liu YR, Wang YZ, Shi HX, Lai YY, Xu LP, Liu DH, Jiang Q, Li LD, Jiang B, Liu KY, Huang XJ (2013) PRAME and WT1 transcripts constitute a good molecular marker combination for monitoring minimal residual disease in myelodysplastic syndromes. Leuk Lymphoma 54(7):1442–1449CrossRef
14.
Zurück zum Zitat Beillard E, Pallisgaard N, van der Velden VH, Bi W, Dee R, van der Schoot E, Delabesse E, Macintyre E, Gottardi E, Saglio G, Watzinger F, Lion T, van Dongen JJ, Hokland P, Gabert J (2003) Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using ‘real-time’ quantitative reverse-transcriptase polymerase chain reaction (RQ-PCR) - a Europe against cancer program. Leukemia 17(12):2474–2486CrossRef Beillard E, Pallisgaard N, van der Velden VH, Bi W, Dee R, van der Schoot E, Delabesse E, Macintyre E, Gottardi E, Saglio G, Watzinger F, Lion T, van Dongen JJ, Hokland P, Gabert J (2003) Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using ‘real-time’ quantitative reverse-transcriptase polymerase chain reaction (RQ-PCR) - a Europe against cancer program. Leukemia 17(12):2474–2486CrossRef
15.
Zurück zum Zitat Caye A, Beldjord K, Mass-Malo K, Drunat S, Soulier J, Gandemer V, Baruchel A, Bertrand Y, Cavé H, Clappier E (2013) Breakpoint-specific multiplex polymerase chain reaction allows the detection of IKZF1 intragenic deletions and minimal residual disease monitoring in B-cell precursor acute lymphoblastic leukemia. Haematologica 98(4):597–601CrossRef Caye A, Beldjord K, Mass-Malo K, Drunat S, Soulier J, Gandemer V, Baruchel A, Bertrand Y, Cavé H, Clappier E (2013) Breakpoint-specific multiplex polymerase chain reaction allows the detection of IKZF1 intragenic deletions and minimal residual disease monitoring in B-cell precursor acute lymphoblastic leukemia. Haematologica 98(4):597–601CrossRef
16.
Zurück zum Zitat Den Boer ML, van Slegtenhorst M, De Menezes RX, Cheok MH, Buijs-Gladdines JG, Peters ST, Van Zutven LJ, Beverloo HB, Van der Spek PJ, Escherich G, Horstmann MA, Janka-Schaub GE, Kamps WA, Evans WE, Pieters R (2009) A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol 10(2):125–134CrossRef Den Boer ML, van Slegtenhorst M, De Menezes RX, Cheok MH, Buijs-Gladdines JG, Peters ST, Van Zutven LJ, Beverloo HB, Van der Spek PJ, Escherich G, Horstmann MA, Janka-Schaub GE, Kamps WA, Evans WE, Pieters R (2009) A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol 10(2):125–134CrossRef
17.
Zurück zum Zitat van der Veer A, Waanders E, Pieters R, Willemse ME, Van Reijmersdal SV, Russell LJ, Harrison CJ, Evans WE, van der Velden VH, Hoogerbrugge PM, Van Leeuwen F, Escherich G, Horstmann MA, Mohammadi Khankahdani L, Rizopoulos D, De Groot-Kruseman HA, Sonneveld E, Kuiper RP, Den Boer ML (2013) Independent prognostic value of BCR-ABL1-like signature and IKZF1 deletion, but not high CRLF2 expression, in children with B-cell precursor ALL. Blood 122(15):2622–2629CrossRef van der Veer A, Waanders E, Pieters R, Willemse ME, Van Reijmersdal SV, Russell LJ, Harrison CJ, Evans WE, van der Velden VH, Hoogerbrugge PM, Van Leeuwen F, Escherich G, Horstmann MA, Mohammadi Khankahdani L, Rizopoulos D, De Groot-Kruseman HA, Sonneveld E, Kuiper RP, Den Boer ML (2013) Independent prognostic value of BCR-ABL1-like signature and IKZF1 deletion, but not high CRLF2 expression, in children with B-cell precursor ALL. Blood 122(15):2622–2629CrossRef
18.
Zurück zum Zitat Foa R, Vitale A, Mancini M, Cuneo A, Mecucci C, Elia L, Lombardo R, Saglio G, Torelli G, Annino L, Specchia G, Damasio E, Recchia A, Di Raimondo F, Morra E, Volpe E, Tafuri A, Fazi P, Hunger SP, Mandelli F (2003) E2A-PBX1 fusion in adult acute lymphoblastic leukaemia: biological and clinical features. Br J Haematol 120(3):484–487CrossRef Foa R, Vitale A, Mancini M, Cuneo A, Mecucci C, Elia L, Lombardo R, Saglio G, Torelli G, Annino L, Specchia G, Damasio E, Recchia A, Di Raimondo F, Morra E, Volpe E, Tafuri A, Fazi P, Hunger SP, Mandelli F (2003) E2A-PBX1 fusion in adult acute lymphoblastic leukaemia: biological and clinical features. Br J Haematol 120(3):484–487CrossRef
19.
Zurück zum Zitat Mancini M, Scappaticci D, Cimino G, Nanni M, Derme V, Elia L, Tafuri A, Vignetti M, Vitale A, Cuneo A, Castoldi G, Saglio G, Pane F, Mecucci C, Camera A, Specchia G, Tedeschi A, Di Raimondo F, Fioritoni G, Fabbiano F, Marmont F, Ferrara F, Cascavilla N, Todeschini G, Nobile F, Kropp MG, Leoni P, Tabilio A, Luppi M, Annino L, Mandelli F, Foà R (2005) A comprehensive genetic classification of adult acute lymphoblastic leukemia (ALL): analysis of the GIMEMA 0496 protocol. Blood 105(9):3434–3441CrossRef Mancini M, Scappaticci D, Cimino G, Nanni M, Derme V, Elia L, Tafuri A, Vignetti M, Vitale A, Cuneo A, Castoldi G, Saglio G, Pane F, Mecucci C, Camera A, Specchia G, Tedeschi A, Di Raimondo F, Fioritoni G, Fabbiano F, Marmont F, Ferrara F, Cascavilla N, Todeschini G, Nobile F, Kropp MG, Leoni P, Tabilio A, Luppi M, Annino L, Mandelli F, Foà R (2005) A comprehensive genetic classification of adult acute lymphoblastic leukemia (ALL): analysis of the GIMEMA 0496 protocol. Blood 105(9):3434–3441CrossRef
20.
Zurück zum Zitat Gleissner B, Goekbuget N, Rieder H, Arnold R, Schwartz S, Diedrich H, Schoch C, Heinze B, Fonatsch C, Bartram CR, Hoelzer D, Thiel E, GMALL Study Group (2005) CD10- pre-B acute lymphoblastic leukemia (ALL) is a distinct high-risk subgroup of adult ALL associated with a high frequency of MLL aberrations: results of the German Multicenter Trials for Adult ALL (GMALL). Blood 106(13):4054–4056CrossRef Gleissner B, Goekbuget N, Rieder H, Arnold R, Schwartz S, Diedrich H, Schoch C, Heinze B, Fonatsch C, Bartram CR, Hoelzer D, Thiel E, GMALL Study Group (2005) CD10- pre-B acute lymphoblastic leukemia (ALL) is a distinct high-risk subgroup of adult ALL associated with a high frequency of MLL aberrations: results of the German Multicenter Trials for Adult ALL (GMALL). Blood 106(13):4054–4056CrossRef
21.
Zurück zum Zitat Issa GC, Kantarjian HM, Yin CC, Qiao W, Ravandi F, Thomas D, Short NJ, Sasaki K, Garcia-Manero G, Kadia TM, Cortes JE, Daver N, Borthakur G, Jain N, Konopleva M, Khouri I, Kebriaei P, Champlin RE, Pierce S, O'Brien SM, Jabbour E (2017) Prognostic impact of pretreatment cytogenetics in adult Philadelphia chromosome-negative acute lymphoblastic leukemia in the era of minimal residual disease. Cancer 123(3):459–467CrossRef Issa GC, Kantarjian HM, Yin CC, Qiao W, Ravandi F, Thomas D, Short NJ, Sasaki K, Garcia-Manero G, Kadia TM, Cortes JE, Daver N, Borthakur G, Jain N, Konopleva M, Khouri I, Kebriaei P, Champlin RE, Pierce S, O'Brien SM, Jabbour E (2017) Prognostic impact of pretreatment cytogenetics in adult Philadelphia chromosome-negative acute lymphoblastic leukemia in the era of minimal residual disease. Cancer 123(3):459–467CrossRef
22.
Zurück zum Zitat Moorman AV, Harrison CJ, Buck GA, Richards SM, Secker-Walker LM, Martineau M, Vance GH, Cherry AM, Higgins RR, Fielding AK, Foroni L, Paietta E, Tallman MS, Litzow MR, Wiernik PH, Rowe JM, Goldstone AH, Dewald GW, Adult Leukaemia Working Party, Medical Research Council/National Cancer Research Institute (2007) Karyotype is an independent prognostic factor in adult acute lymphoblastic leukemia (ALL): analysis of cytogenetic data from patients treated on the Medical Research Council (MRC) UKALLXII/Eastern Cooperative Oncology (ECOG) 2993 trial. Blood 109(8):3189–3197CrossRef Moorman AV, Harrison CJ, Buck GA, Richards SM, Secker-Walker LM, Martineau M, Vance GH, Cherry AM, Higgins RR, Fielding AK, Foroni L, Paietta E, Tallman MS, Litzow MR, Wiernik PH, Rowe JM, Goldstone AH, Dewald GW, Adult Leukaemia Working Party, Medical Research Council/National Cancer Research Institute (2007) Karyotype is an independent prognostic factor in adult acute lymphoblastic leukemia (ALL): analysis of cytogenetic data from patients treated on the Medical Research Council (MRC) UKALLXII/Eastern Cooperative Oncology (ECOG) 2993 trial. Blood 109(8):3189–3197CrossRef
23.
Zurück zum Zitat Boublikova L, Kalinova M, Ryan J, Quinn F, O'Marcaigh A, Smith O, Browne P, Stary J, McCann SR, Trka J, Lawler M (2006) Wilms’ tumor gene 1 (WT1) expression in childhood acute lymphoblastic leukemia: a wide range of WT1 expression levels, its impact on prognosis and minimal residual disease monitoring. Leukemia 20(2):254–263CrossRef Boublikova L, Kalinova M, Ryan J, Quinn F, O'Marcaigh A, Smith O, Browne P, Stary J, McCann SR, Trka J, Lawler M (2006) Wilms’ tumor gene 1 (WT1) expression in childhood acute lymphoblastic leukemia: a wide range of WT1 expression levels, its impact on prognosis and minimal residual disease monitoring. Leukemia 20(2):254–263CrossRef
24.
Zurück zum Zitat Heesch S, Goekbuget N, Stroux A, Tanchez JO, Schlee C, Burmeister T, Schwartz S, Blau O, Keilholz U, Busse A, Hoelzer D, Thiel E, Hofmann WK, Baldus CD (2010) Prognostic implications of mutations and expression of the Wilms tumor 1 (WT1) gene in adult acute T-lymphoblastic leukemia. Haematologica 95(6):942–949CrossRef Heesch S, Goekbuget N, Stroux A, Tanchez JO, Schlee C, Burmeister T, Schwartz S, Blau O, Keilholz U, Busse A, Hoelzer D, Thiel E, Hofmann WK, Baldus CD (2010) Prognostic implications of mutations and expression of the Wilms tumor 1 (WT1) gene in adult acute T-lymphoblastic leukemia. Haematologica 95(6):942–949CrossRef
25.
Zurück zum Zitat Hughes T, Deininger M, Hochhaus A, Branford S, Radich J, Kaeda J, Baccarani M, Cortes J, Cross NC, Druker BJ, Gabert J, Grimwade D, Hehlmann R, Kamel-Reid S, Lipton JH, Longtine J, Martinelli G, Saglio G, Soverini S, Stock W, Goldman JM (2006) Monitoring CML patients responding to treatment with tyrosine kinase inhibitors: review and recommendations for harmonizing current methodology for detecting BCR-ABL transcripts and kinase domain mutations and for expressing results. Blood 108(1):28–37CrossRef Hughes T, Deininger M, Hochhaus A, Branford S, Radich J, Kaeda J, Baccarani M, Cortes J, Cross NC, Druker BJ, Gabert J, Grimwade D, Hehlmann R, Kamel-Reid S, Lipton JH, Longtine J, Martinelli G, Saglio G, Soverini S, Stock W, Goldman JM (2006) Monitoring CML patients responding to treatment with tyrosine kinase inhibitors: review and recommendations for harmonizing current methodology for detecting BCR-ABL transcripts and kinase domain mutations and for expressing results. Blood 108(1):28–37CrossRef
26.
Zurück zum Zitat Pfeifer H, Cazzaniga G, van der Velden VHJ, Cayuela JM, Schäfer B, Spinelli O, Akiki S, Avigad S, Bendit I, Borg K, Cavé H, Elia L, Reshmi SC, Gerrard G, Hayette S, Hermanson M, Juh A, Jurcek T, Chillón MC, Homburg C, Martinelli G, Kairisto V, Lange T, Lion T, Mueller MC, Pane F, Rai L, Damm-Welk C, Sacha T, Schnittger S, Touloumenidou T, Valerhaugen H, Vandenberghe P, Zuna J, Serve H, Herrmann E, Markovic S, Dongen JJMV, Ottmann OG (2019) Standardisation and consensus guidelines for minimal residual disease assessment in Philadelphia-positive acute lymphoblastic leukemia (Ph + ALL) by real-time quantitative reverse transcriptase PCR of e1a2 BCR-ABL1. Leukemia 33(8):1910–1922CrossRef Pfeifer H, Cazzaniga G, van der Velden VHJ, Cayuela JM, Schäfer B, Spinelli O, Akiki S, Avigad S, Bendit I, Borg K, Cavé H, Elia L, Reshmi SC, Gerrard G, Hayette S, Hermanson M, Juh A, Jurcek T, Chillón MC, Homburg C, Martinelli G, Kairisto V, Lange T, Lion T, Mueller MC, Pane F, Rai L, Damm-Welk C, Sacha T, Schnittger S, Touloumenidou T, Valerhaugen H, Vandenberghe P, Zuna J, Serve H, Herrmann E, Markovic S, Dongen JJMV, Ottmann OG (2019) Standardisation and consensus guidelines for minimal residual disease assessment in Philadelphia-positive acute lymphoblastic leukemia (Ph + ALL) by real-time quantitative reverse transcriptase PCR of e1a2 BCR-ABL1. Leukemia 33(8):1910–1922CrossRef
27.
Zurück zum Zitat Willasch AM, Gruhn B, Coliva T, Kalinova M, Schneider G, Kreyenberg H, Steinbach D, Weber G, Hollink IH, Zwaan CM, Biondi A, van der Velden VH, Reinhardt D, Cazzaniga G, Bader P, Trka J, European Study Group on WT1 Expression in Childhood AML (2009) Standardization of WT1 mRNA quantitation for minimal residual disease monitoring in childhood AML and implications of WT1 gene mutations: a European multicenter study. Leukemia 23(8):1472–1479CrossRef Willasch AM, Gruhn B, Coliva T, Kalinova M, Schneider G, Kreyenberg H, Steinbach D, Weber G, Hollink IH, Zwaan CM, Biondi A, van der Velden VH, Reinhardt D, Cazzaniga G, Bader P, Trka J, European Study Group on WT1 Expression in Childhood AML (2009) Standardization of WT1 mRNA quantitation for minimal residual disease monitoring in childhood AML and implications of WT1 gene mutations: a European multicenter study. Leukemia 23(8):1472–1479CrossRef
28.
Zurück zum Zitat Yang L, Han Y, Suarez Saiz F, Minden MD (2007) A tumor suppressor and oncogene: the WT1 story. Leukemia 21(5):868–876CrossRef Yang L, Han Y, Suarez Saiz F, Minden MD (2007) A tumor suppressor and oncogene: the WT1 story. Leukemia 21(5):868–876CrossRef
29.
Zurück zum Zitat Marlton P (2014) The many facets of WT1 in acute myeloid leukemia: clarity remains elusive. Leuk Lymphoma 55(2):235–237CrossRef Marlton P (2014) The many facets of WT1 in acute myeloid leukemia: clarity remains elusive. Leuk Lymphoma 55(2):235–237CrossRef
Metadaten
Titel
The prognostic significance of Wilms’ tumor gene 1 (WT1) expression at diagnosis in adults with Ph-negative B cell precursor acute lymphoblastic leukemia
verfasst von
Ya-Zhen Qin
Qian Jiang
Lan-Ping Xu
Hao Jiang
Yu Wang
Xiao-Su Zhao
Zong-Ru Li
Yue-Yun Lai
Yan-Rong Liu
Xiao-Hui Zhang
Kai-Yan Liu
Xiao-Jun Huang
Publikationsdatum
06.09.2019
Verlag
Springer Berlin Heidelberg
Erschienen in
Annals of Hematology / Ausgabe 11/2019
Print ISSN: 0939-5555
Elektronische ISSN: 1432-0584
DOI
https://doi.org/10.1007/s00277-019-03789-6

Weitere Artikel der Ausgabe 11/2019

Annals of Hematology 11/2019 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.