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Articles

Adult acute myeloid leukemia patients with NUP98 rearrangement have frequent cryptic translocations and unfavorable outcome

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Pages 1907-1916 | Received 11 Oct 2021, Accepted 16 Feb 2022, Published online: 08 Mar 2022

References

  • Shallis RM, Wang R, Davidoff A, et al. Epidemiology of acute myeloid leukemia: recent progress and enduring challenges. Blood Rev. 2019;36:70–87.
  • Cancer stat facts: Leukemia—acute myeloid leukemia (AML). https://seer.cancer.gov/statfacts/html/amyl.html
  • Slape C, Aplan PD. The role of NUP98 gene fusions in hematologic malignancy. Leuk Lymphoma. 2004;45(7):1341–1350.
  • Michmerhuizen NL, Klco JM, Mullighan CG. Mechanistic insights and potential therapeutic approaches for NUP98-rearranged hematologic malignancies. Blood. 2020;136(20):2275–2289.
  • Kalverda B, Pickersgill H, Shloma VV, et al. Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell. 2010;140(3):360–371.
  • Franks TM, Hetzer MW. The role of Nup98 in transcription regulation in healthy and diseased cells. Trends Cell Biol. 2013;23(3):112–117.
  • Laurell E, Beck K, Krupina K, et al. Phosphorylation of Nup98 by multiple kinases is crucial for NPC disassembly during mitotic entry. Cell. 2011;144(4):539–550.
  • Capelson M, Liang Y, Schulte R, et al. Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell. 2010;140(3):372–383.
  • Tomiyasu T, Sasaki M, Kondo K, et al. Chromosome banding studies in 106 cases of chronic myelogenous leukemia. Jinrui Idengaku Zasshi. 1982;27(3):243–258.
  • Nakamura T, Largaespada DA, Lee MP, et al. Fusion of the nucleoporin gene NUP98 to HOXA9 by the chromosome translocation t(7;11)(p15;p15) in human myeloid leukaemia. Nat Genet. 1996;12(2):154–158.
  • Borrow J, Shearman AM, Stanton VP Jr, et al. The t(7;11)(p15;p15) translocation in acute myeloid leukaemia fuses the genes for nucleoporin NUP98 and class I homeoprotein HOXA9. Nat Genet. 1996;12(2):159–167.
  • Xu S, Powers MA. Nuclear pore proteins and cancer. Semin Cell Dev Biol. 2009;20(5):620–630.
  • Radu A, Moore MS, Blobel G. The peptide repeat domain of nucleoporin Nup98 functions as a docking site in transport across the nuclear pore complex. Cell. 1995;81(2):215–222.
  • Griffis ER, Altan N, Lippincott-Schwartz J, et al. Nup98 is a mobile nucleoporin with transcription-dependent dynamics. Mol Biol Cell. 2002;13(4):1282–1297.
  • Gough SM, Slape CI, Aplan PD. NUP98 gene fusions and hematopoietic malignancies: common themes and new biologic insights. Blood. 2011;118(24):6247–6257.
  • Blevins MB, Smith AM, Phillips EM, et al. Complex formation among the RNA export proteins Nup98, Rae1/Gle2, and TAP. J Biol Chem. 2003;278(23):20979–20988.
  • Terlecki-Zaniewicz S, Humer T, Eder T, et al. Biomolecular condensation of NUP98 fusion proteins drives leukemogenic gene expression. Nat Struct Mol Biol. 2021;28(2):190–201.
  • Struski S, Lagarde S, Bories P, et al. NUP98 is rearranged in 3.8% of pediatric AML forming a clinical and molecular homogenous group with a poor prognosis. Leukemia. 2017;31(3):565–572.
  • Quessada J, Cuccuini W, Saultier P, et al. Cytogenetics of pediatric acute myeloid leukemia: a review of the current knowledge. Genes (Basel). 2021;12(6):924.
  • Chou WC, Chen CY, Hou HA, et al. Acute myeloid leukemia bearing t(7;11)(p15;p15) is a distinct cytogenetic entity with poor outcome and a distinct mutation profile: comparative analysis of 493 adult patients. Leukemia. 2009;23(7):1303–1310.
  • Fasan A, Haferlach C, Alpermann T, et al. A rare but specific subset of adult AML patients can be defined by the cytogenetically cryptic NUP98-NSD1 fusion gene. Leukemia. 2013;27(1):245–248.
  • Thol F, Kolking B, Hollink IH, et al. Analysis of NUP98/NSD1 translocations in adult AML and MDS patients. Leukemia. 2013;27(3):750–754.
  • Wei S, Wang S, Qiu S, et al. Clinical and laboratory studies of 17 patients with acute myeloid leukemia harboring t(7;11)(p15;p15) translocation. Leuk Res. 2013;37(9):1010–1015.
  • Mrozek K, Marcucci G, Nicolet D, et al. Prognostic significance of the European LeukemiaNet standardized system for reporting cytogenetic and molecular alterations in adults with acute myeloid leukemia. J Clin Oncol. 2012;30(36):4515–4523.
  • Ley TJ, Miller C, Ding L, et al. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med. 2013;368(22):2059–2074.
  • Press RD, Eickelberg G, Froman A, et al. Next-generation sequencing-defined minimal residual disease before stem cell transplantation predicts acute myeloid leukemia relapse. Am J Hematol. 2019;94(8):902–912.
  • Newell LF, Williams T, Liu J, et al. Engrafted donor-derived clonal hematopoiesis after allogenic hematopoietic cell transplantation is associated with chronic graft-versus-host disease requiring immunosuppressive therapy, but no adverse impact on overall survival or relapse. Transplant Cell Ther. 2021;27:662.e1–662.e9.
  • Ma J, Dunlap J, Paliga A, et al. DNMT3A co-mutation is required for FLT3-ITD as an adverse prognostic indicator in intermediate-risk cytogenetic group AML. Leuk Lymphoma. 2018;59(8):1938–1948.
  • de Rooij JD, Hollink IH, Arentsen-Peters ST, et al. NUP98/JARID1A is a novel recurrent abnormality in pediatric acute megakaryoblastic leukemia with a distinct HOX gene expression pattern. Leukemia. 2013;27(12):2280–2288.
  • Iacobucci I, Wen J, Meggendorfer M, et al. Genomic subtyping and therapeutic targeting of acute erythroleukemia. Nat Genet. 2019;51(4):694–704.
  • Noort S, Wander P, Alonzo TA, et al. The clinical and biological characteristics of NUP98-KDM5A in pediatric acute myeloid leukemia. Haematologica. 2021;106(2):630–634.
  • Moore MA, Chung KY, Plasilova M, et al. NUP98 dysregulation in myeloid leukemogenesis. Ann N Y Acad Sci. 2007;1106:114–142.
  • Burillo-Sanz S, Morales-Camacho RM, Caballero-Velazquez T, et al. NUP98-HOXA9 bearing therapy-related myeloid neoplasm involves myeloid-committed cell and induces HOXA5, EVI1, FLT3, and MEIS1 expression. Int J Lab Hematol. 2016;38(1):64–71.
  • Block AW, Carroll AJ, Hagemeijer A, et al. Rare recurring balanced chromosome abnormalities in therapy-related myelodysplastic syndromes and acute leukemia: report from an international workshop. Genes Chromosomes Cancer. 2002;33(4):401–412.
  • Togni M, Masetti R, Pigazzi M, et al. Identification of the NUP98-PHF23 fusion gene in pediatric cytogenetically normal acute myeloid leukemia by whole-transcriptome sequencing. J Hematol Oncol. 2015;8:69.
  • Ning Y. A cryptic translocation leading to NUP98-PHF23 fusion in AML. Best Pract Res Clin Haematol. 2016;29(4):320–323.
  • Hollink IH, van den Heuvel-Eibrink MM, Arentsen-Peters ST, et al. NUP98/NSD1 characterizes a novel poor prognostic group in acute myeloid leukemia with a distinct HOX gene expression pattern. Blood. 2011;118(13):3645–3656.
  • Dohner H, Estey E, Grimwade D, et al. Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel. Blood. 2017;129(4):424–447.
  • Haferlach C, Bacher U, Grossmann V, et al. Three novel cytogenetically cryptic EVI1 rearrangements associated with increased EVI1 expression and poor prognosis identified in 27 acute myeloid leukemia cases. Genes Chromosomes Cancer. 2012;51(12):1079–1085.
  • Bolouri H, Farrar JE, Triche T Jr, et al. The molecular landscape of pediatric acute myeloid leukemia reveals recurrent structural alterations and age-specific mutational interactions. Nat Med. 2018;24(1):103–112.
  • Ostronoff F, Othus M, Gerbing RB, et al. NUP98/NSD1 and FLT3/ITD coexpression is more prevalent in younger AML patients and leads to induction failure: a COG and SWOG report. Blood. 2014;124(15):2400–2407.
  • Niktoreh N, Walter C, Zimmermann M, et al. Mutated WT1, FLT3-ITD, and NUP98-NSD1 fusion in various combinations define a poor prognostic group in pediatric acute myeloid leukemia. J Oncol. 2019;2019:1–15.
  • Thanasopoulou A, Tzankov A, Schwaller J. Potent co-operation between the NUP98-NSD1 fusion and the FLT3-ITD mutation in acute myeloid leukemia induction. Haematologica. 2014;99(9):1465–1471.
  • Mohanty S, Jyotsana N, Sharma A, et al. Targeted inhibition of the NUP98-NSD1 fusion oncogene in acute myeloid leukemia. Cancers (Basel). 2020;12(10):2766.

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