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Acute myeloid leukemia

RUNX1 mutations in acute myeloid leukemia are associated with distinct clinico-pathologic and genetic features

Leukemia volume 30, pages 2160–2168 (2016)Cite this article

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A Corrigendum to this article was published on 02 November 2016

Abstract

We evaluated the frequency, genetic architecture, clinico-pathologic features and prognostic impact of RUNX1 mutations in 2439 adult patients with newly-diagnosed acute myeloid leukemia (AML). RUNX1 mutations were found in 245 of 2439 (10%) patients; were almost mutually exclusive of AML with recurrent genetic abnormalities; and they co-occurred with a complex pattern of gene mutations, frequently involving mutations in epigenetic modifiers (ASXL1, IDH2, KMT2A, EZH2), components of the spliceosome complex (SRSF2, SF3B1) and STAG2, PHF6, BCOR. RUNX1 mutations were associated with older age (16–59 years: 8.5%; ⩾60 years: 15.1%), male gender, more immature morphology and secondary AML evolving from myelodysplastic syndrome. In univariable analyses, RUNX1 mutations were associated with inferior event-free (EFS, P<0.0001), relapse-free (RFS, P=0.0007) and overall survival (OS, P<0.0001) in all patients, remaining significant when age was considered. In multivariable analysis, RUNX1 mutations predicted for inferior EFS (P=0.01). The effect of co-mutation varied by partner gene, where patients with the secondary genotypes RUNX1mut/ASXL1mut (OS, P=0.004), RUNX1mut/SRSF2mut (OS, P=0.007) and RUNX1mut/PHF6mut (OS, P=0.03) did significantly worse, whereas patients with the genotype RUNX1mut/IDH2mut (OS, P=0.04) had a better outcome. In conclusion, RUNX1-mutated AML is associated with a complex mutation cluster and is correlated with distinct clinico-pathologic features and inferior prognosis.

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Acknowledgements

Supported in part by grants 01GI9981 and 01KG0605 from the German Bundesministerium für Bildung und Forschung (BMBF), grant 109675 from the Deutsche Krebshilfe and the Sonderforschungsbereich (SFB) 1074 funded by the Deutsche Forschungsgemeinschaft (SFB 1074, projects B3 and B4). VG is a grant recipient of the Medical Faculty of Ulm University; LB and MH are Heisenberg Professors of the Deutsche Forschungsgemeinschaft (DFG, BU 1339/3-8 and HE 5240-6-1). HAK is in part supported by Deutsche Forschungsgemeinschaft (SFB 1074, project Z1), German Bundesministerium für Bildung und Forschung (BMBF; Gerontosys II, Forschungskern SyStaR, project ID 0315894); European Community's Seventh Framework Programme (FP7/2007-2013) under grant agreement nº 602783. AMLSG treatment trials were in part supported by Pfizer and Amgen. We are grateful to all members of the German-Austrian AML Study Group (AMLSG) for their participation in this study and providing patient samples; a list of participating institutions and investigators appears in the Supplementary information.

Author contributions

VIG, VT, RFS, KD and HD designed the research; VIG, VT, EP, PP, JH, TW and BK performed experiments; VIG, VT, EP, PP, JH, BS, TW, BK and KD analyzed results; DW, MG, JMK, HAK and RFS performed statistical analyses; CHK, HAH, PB, GH, AK, M Ringhoffer, KG, M Rummel, FT, MH, AG, LB, RFS, KD and HD accrued patients and provided material; VIG, VT, EP, RFS, KD and HD wrote the paper.

Author information

Author notes

  1. V I Gaidzik, V Teleanu, E Papaemmanuil, D Weber, P Paschka, J Hahn, T Wallrabenstein, B Kolbinger, C H Köhne, H A Horst, P Brossart, G Held, A Kündgen, M Ringhoffer, K Götze, M Rummel, M Gerstung, P Campbell, J M Kraus, H A Kestler, F Thol, M Heuser, B Schlegelberger, A Ganser, L Bullinger, R F Schlenk, K Döhner and H Döhner: V I Gaidzik and V Teleanu: These authors contributed equally to this work.

  2. A complete list of the members of the German-Austrian Acute Myeloid Leukemia Study Group (AMLSG) appears in the 'Supplementary information'.

Authors and Affiliations

  1. Klinik für Innere Medizin III, Universitätsklinikum Ulm, Ulm, Germany

    V I Gaidzik, V Teleanu, D Weber, P Paschka, J Hahn, T Wallrabenstein, B Kolbinger, L Bullinger, R F Schlenk, K Döhner & H Döhner

  2. Cancer Genome Project, Wellcome Trust Sanger Institute, Cambridge, UK

    E Papaemmanuil, M Gerstung & P Campbell

  3. Klinik für Hämatologie und Onkologie, Klinikum Oldenburg, Oldenburg, Germany

    C H Köhne

  4. Klinik für Innere Medizin II, Universitätsklinikum Schleswig-Holstein Campus Kiel, Kiel, Germany

    H A Horst

  5. Medizinische Klinik und Poliklinik III, Universitätsklinikum Bonn, Bonn, Germany

    P Brossart

  6. Klinik für Innere Medizin I, Universitätskliniken des Saarlandes, Homburg, Germany

    G Held

  7. Klinik für Hämatologie, Onkologie und Klinische Onkologie, Universitätsklinikum Düsseldorf, Düsseldorf, Germany

    A Kündgen

  8. Medizinische Klinik III, Städtisches Klinikum Karlsruhe gGmbH, Karlsruhe, Germany

    M Ringhoffer

  9. III. Medizinische Klinik, Klinikum Rechts der Isar, Technische Universität München, München, Germany

    K Götze

  10. Medizinische Klinik IV, Universitätsklinikum Gießen, Gießen, Germany

    M Rummel

  11. Medical Systems Biology, Universität Ulm, Ulm, Germany

    J M Kraus & H A Kestler

  12. Klinik für Hämatologie, Hämostaseologie, Onkologie und Stammzelltransplantation, Medizinische Hochschule Hannover, Hannover, Germany

    F Thol, M Heuser, B Schlegelberger & A Ganser

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  1. V I Gaidzik
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Gaidzik, V., Teleanu, V., Papaemmanuil, E. et al. RUNX1 mutations in acute myeloid leukemia are associated with distinct clinico-pathologic and genetic features. Leukemia 30, 2160–2168 (2016). https://doi.org/10.1038/leu.2016.126

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