NUP98-NSD1 fusion in association with FLT3-ITD mutation identifies a prognostically relevant subgroup of pediatric acute myeloid leukemia patients suitable for monitoring by real time quantitative PCR

Genes Chromosomes and Cancer

Volumn 52, Issue 11, 2013, Pages 1053-1064

  Akiki, Susanna ^a,b   Dyer, Sara A ^a,b   Grimwade, David ^c   Ivey, Adam ^c,d   Abou Zeid, Nervana ^a   Borrow, Julian ^a,b   Jeffries, Sally ^a   Caddick, Judith ^a   Newell, Hayley ^a   Begum, Suriya ^a   Tawana, Kiran ^e   Mason, Joanne ^a   Velangi, Mark ^e   Griffiths, Michael ^a,b  

^a BIRMINGHAM CHILDREN S HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d Molecular Diagnostics   (United Kingdom)

^e BIRMINGHAM CHILDREN S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; CISPLATIN; CLOFARABINE; CYCLOPHOSPHAMIDE; CYTARABINE; DAUNORUBICIN; DOXORUBICIN; ETOPOSIDE; FLUDARABINE; GEMTUZUMAB OZOGAMICIN; GRANULOCYTE COLONY STIMULATING FACTOR; IDARUBICIN; METHOTREXATE;

ACUTE GRANULOCYTIC LEUKEMIA; ADOLESCENT; ADULT; ARTICLE; CANCER PROGNOSIS; CEBPA GENE; CHILD; CONTROLLED STUDY; CYTOGENETICS; FEMALE; FLT3 GENE; GENE; GENE FUSION; GENE MUTATION; GENE REARRANGEMENT; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SCREENING; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; INFANT; INTERNAL TANDEM DUPLICATION; MAJOR CLINICAL STUDY; MALE; NPM1 GENE; NSD1 GENE; NUCLEOTIDE SEQUENCE; NUP98 GENE; PRESCHOOL CHILD; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHOOL CHILD; TREATMENT RESPONSE;

EID: 84884699891     PISSN: 10452257     EISSN: 10982264     Source Type: Journal    
DOI: 10.1002/gcc.22100     Document Type: Article

References (31)

1. Balgobind BV, Hollink IH, Arentsen-Peters ST, Zimmermann M, Harbott J, Beverloo HB, von Bergh AR, Cloos J, Kaspers GJ, de Haas V, Zemanova Z, Stary J, Cayuela J-M, Baruchel A, Creutzig U, Reinhardt D, Pieters R, Zwaan CM, van den Heuvel-Eibrink MM. 2011. Integrative analysis of type-I and type-II aberrations underscores the genetic heterogeneity of pediatric acute myeloid leukemia. Haematologica 96:1478-1487.
2. Benthaus T, Schneider F, Mellert G, Zellmeier E, Schneider S, Kakadia PM, Hiddemann W, Bohlander SK, Feuring-Buske M, Braess J, Spiekermann K, Dufour A. 2008. Rapid and sensitive screening for CEBPA mutations in acute myeloid leukaemia. Br J Haematol 143:230-239.
3. Borrow J, Shearman AM, Stanton VP, Becher R, Collins T, Williams AJ, Dubé I, Katz F, Kwong YL, Morris C, Ohyashiki K, Toyama K, Rowley J, Housman DE. 1996. The t(7;11)(p15;p15) translocation in acute myeloid leukaemia fuses the genes for nucleoporin NUP98 and class I homeoprotein HOXA9. Nat Genet 12:159-167.
4. Brown J, Jawad M, Twigg SR, Saracoglu K, Sauerbrey A, Thomas A, Eils R, Harbott J, Kearney L. 2002. A cryptic t(5;11) (q35;p15.5) in 2 children with acute myeloid leukemia with apparently normal karyotypes, identified by a multiplex fluorescence in situ hybridization telomere assay. Blood 99:2526-2531.
5. Cerveira N, Correia C, Dória S, Bizarro S, Rocha P, Gomes P, Torres L, Norton L, Borges BS, Castedo S, Teixeira MR. 2003. Frequency of NUP98/NSD1 fusion transcript in childhood acute myeloid leukaemia. Leukemia 17:2244-2247.
6. Cheson BD, Bennett JM, Kopecky KJ, Büchner T, Willman CL, Estey EH, Schiffer CA, Doehner H, Tallman MS, Lister TA, Lo-Coco F, Willemze R, Biondi A, Hiddemann W, Larson RA, Löwenberg B, Sanz MA, Head DR, Ohno R, Bloomfield CD. 2003. Revised recommendations of the international working group for diagnosis, standardization of response criteria, treatment outcomes, and reporting standards for therapeutic trials in acute myeloid leukemia. J Clin Oncol 21:4642-4649.
7. Flora R, Grimwade D. 2004. Real-time quantitative RT-PCR to detect fusion gene transcripts associated with AML. Methods Mol Med 91:151-173.
8. Freeman SD, Jovanovic JV, Grimwade D. 2008. Development of minimal residual disease-directed therapy in acute myeloid leukemia. Sem Oncol 35:388-400.
9. Gabert J, Beillard E, van der Velden VH, Bi W, Grimwade D, Pallisgaard N, Barbany G, Cazzaniga G, Cayuela JM, Cavé H, Pane F, Aerts JL, De Micheli D, Thirion X, Pradel V, González M, Viehmann S, Malec M, Saglio G, van Dongen JJ. 2003. Standardization and quality control studies of 'real-time' quantitative reverse transcriptase polymerase chain reaction of fusion gene transcripts for residual disease detection in leukemia-A Europe Against Cancer program. Leukemia 17:2318-2357.
10. Gough SM, Slape CI, Aplan PD. 2011. NUP98 gene fusions and hematopoietic malignancies: Common themes and new biologic insights. Blood 118:6247-6257.
11. Griffiths M, Mason J, Rindl M, Akiki S, McMullan D, Stinton V, Powell H, Curtis A, Bown N, Craddock C. 2005. Acquired isodisomy for chromosome 13 is common in AML, and associated with FLT3-itd mutations. Leukemia 19:2355-2358.
12. Grimwade D, Jovanovic JV, Hills RK, Nugent EA, 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. 2009. Prospective minimal residual disease monitoring to predict relapse of acute promyelocytic leukemia and to direct pre-emptive arsenic trioxide therapy. J Clin Oncol 27:3650-3658.
13. Grimwade D, Hills RK, Moorman AV, Walker H, Chatters S, Goldstone AH, Wheatley K, Harrison CJ, Burnett AK. 2010. 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 116:354-365.
14. Harrison CJ, Hills RK, Moorman AV, Grimwade DJ, Hann I, Webb DK, Wheatley K, de Graaf SS, van den Berg E, Burnett AK, Gibson BE. 2010. Cytogenetics of childhood acute myeloid leukaemia: United Kingdom Medical Research Council Treatment trials AML10 and 12. J Clin Oncol 28:2674-2681.
15. Hollink IH, van den Heuvel-Eibrink MM, Arentsen-Peters ST, Pratcorona M, Abbas S, Kuipers JE, van Galen JF, Beverloo HB, Sonneveld E, Kaspers G-J, Trka J, Baruchel A, Zimmermann M, Creutzig U, Reinhardt D, Pieters R, Valk PJ, Zwaan CM. 2011. NUP98/NSD1 characterizes a novel poor prognostic group in acute myeloid leukemia with a distinct HOX gene expression pattern. Blood 118:3645-3656.
16. Jaju RJ, Haas OA, Neat M, Harbott J, Saha V, Boultwood J, Brown JM, Pirc-Danoewinata H, Krings BW, Müller U, Morris SW, Wainscoat JS, Kearney L. 1999. A new recurrent translocation, t(5;11)(q35;p15.5), associated with del(5q) in childhood acute myeloid leukemia. Blood 94:773-780.
17. Jaju RJ, Fidler C, Haas OA, Strickson AJ, Watkins F, Clark K, Cross NC, Cheng J-F, Aplan PD, Kearney L, Boultwood J, Wainscoat, JS. 2001. A novel gene, NSD1, is fused to NUP98 in the t(5;11)(q35;p15.5) in de novo childhood acute myeloid leukemia. Blood 98:1264-1267.
18. Kaspers GJ, Creutzig U. 2005. Pediatric acute myeloid leukemia: International progress and future directions. Leukemia 19:2025-2029.
19. Kottaridis PD, Gale RE, Frew ME, Harrison G, Langabeer SE, Belton AA, Walker H, Wheatley K, Bowen DT, Burnett AK, Goldstone AH, Linch DC. 2001. The presence of a FLT3 internal tandem duplication in patients with acute myeloid leukemia (AML) adds important prognostic information to cytogenetic risk group and response to the first cycle of chemotherapy: Analysis of 854 patients from the United Kingdom Medical Research Council AML 10 and 12 trials. Blood 98:1752-1759.
20. Meshinchi S, Alonzo TA, Stirewalt DL, Zwaan M, Zimmerman M, Reinhardt D, Kaspers GJ, Heerema NA, Gerbing R, Lange BJ, Radich JP. 2006. Clinical implications of FLT3 mutations in pediatric AML. Blood 108:3654-3661.
21. Mrózek M, Marcucci G, Paschka P, Whitman SP, Bloomfield CD. 2007. 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 109:431-448.
22. Nakamura, T. 2005. NUP98 fusion in human leukemia: Dysregulation of the nuclear pore and homeodomain proteins. Int J Hematol 82:21-27.
23. Nebral K, König M, Schmidt HH, Lutz D, Sperr WR, Kalwak K, Brugger S, Dworzak MN, Haas OA, Strehl S. 2005. Screening for NUP98 rearrangements in hematopoietic malignancies by fluorescence in situ hybridization. Haematologica 90:746-752.
24. Ofran Y, Rowe JM. 2013. Genetic profiling in acute myeloid leukaemia-Where are we and what is its role in patient management. Br J Haematol 160:303-320
25. Panarello C, Rosanda C, Morerio C. 2002. Cryptic translocation t(5;11)(q35;p15.5) with involvement of the NSD1 and NUP98 genes without 5q deletion in childhood acute myeloid leukemia. Genes Chromosomes Cancer 35:277-281.
26. Petit A, Radford I, Waill M-C, Romana S, Berger R. 2008. NUP98-NSD1 fusion by insertion in acute myeloblastic leukemia. Cancer Genet Cytogenet 180:43-46.
27. Radtke I, Mullighan CG, Ishii M, Su X, Cheng J, Ma J, Ganti R, Cai Z, Goorha S, Pounds SB, Cao X, Obert C, Armstrong J, Zhang J, Song G, Ribeiro RC, Rubnitz JE, Raimondi SC, Shurtleff SA, Downing JR. 2009. Genomic analysis reveals few genetic alterations in pediatric acute myeloid leukemia. Proc Natl Acad Sci USA 106:12944-12949.
28. 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; German-Austrian Acute Myeloid Leukemia Study Group. 2008. Mutations and treatment outcome in cytogenetically normal acute myeloid leukemia. N Eng J Med 358:1909-1918.
29. Strehl S, König M, Mann G, Haas OA. 2001. Multiplex reverse transcriptase-polymerase chain reaction screening in childhood acute myeloblastic leukemia. Blood 97:805-808.
30. Taketani T, Taki T, Nakamura T, Kobayashi Y, Ito E, Fukuda S, Yamaguchi S, Hayashi Y. 2010. High frequencies of simultaneous FLT3-ITD, WT1 and KIT mutations in hematological malignancies with NUP98-fusion genes. Leukemia 24:1975-1977.
31. Thiede C, Steudel C, Mohr B, Schaich M, Schäkel U, Platzbecker U, Wermke M, Bornhäuser M, Ritter M, Neubauer A, Ehninger G, Illmer T. 2002. Analysis of FLT3-activating mutations in 979 patients with acute myelogenous leukemia: Association with FAB subtypes and identification of subgroups with poor prognosis. Blood 99:4326-4335.