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Acute myeloid leukemia

GFI1 as a novel prognostic and therapeutic factor for AML/MDS

Leukemia volume 30, pages 1237–1245 (2016)Cite this article

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Abstract

Genetic and epigenetic aberrations contribute to the initiation and progression of acute myeloid leukemia (AML). GFI1, a zinc-finger transcriptional repressor, exerts its function by recruiting histone deacetylases to target genes. We present data that low expression of GFI1 is associated with an inferior prognosis of AML patients. To elucidate the mechanism behind this, we generated a humanized mouse strain with reduced GFI1 expression (GFI1-KD). Here we show that AML development induced by onco-fusion proteins such as MLL-AF9 or NUP98-HOXD13 is accelerated in mice with low human GFI1 expression. Leukemic cells from animals that express low levels of GFI1 show increased H3K9 acetylation compared to leukemic cells from mice with normal human GFI1 expression, resulting in the upregulation of genes involved in leukemogenesis. We investigated a new epigenetic therapy approach for this subgroup of AML patients. We could show that AML blasts from GFI1-KD mice and from AML patients with low GFI1 levels were more sensitive to treatment with histone acetyltransferase inhibitors than cells with normal GFI1 expression levels. We suggest therefore that GFI1 has a dose-dependent role in AML progression and development. GFI1 levels are involved in epigenetic regulation, which could open new therapeutic approaches for AML patients.

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Acknowledgements

We thank all patients for agreeing to participate in the different studies. We thank Saskia Grunwald and Renata Köster for excellent technical assistance and the team of the animal facility of University Hospital Essen for genotyping, technical and administrative assistance during the whole project. We thank Joachim Göthert, Bob Löwenberg, Peter Valk and Lucio Castilla for sharing resources, mice, technical information and patient data. The MCSV-MLL-AF9-IRES-GFP construct was kindly provided by Jay Hess and Lee Grimes. Cyrus Khandanpour was supported by a Max Eder Grant from the Deutsche Krebshilfe, Germany. Tarik Möröy’s lab was supported by a grant from the Canadian Institute for Health Research (MOP – 111011) and by the Leukemia & Lymphoma Society (LLS) and holds a Tier1 Canada Research Chair.

Author contributions

CK, TM. Methodology: CK, TM. Investigation: CK, TM, JMH, LB, HM, AH, CV, LV, FR,TR, BG, AG, SvdCC, YSA-M, AT, SMH, JS, RFL, JF, KL, BP, LKH, MH, GE, CT, UD. Writing Original Draft: CK, JMH, TM, LB, CV, AH. Writing & Editing: CK, JMH, TR, TM. Funding Acquisition: CK, JM, TM, UD, JR. Resources: CK, JM, TM, UD, CT, GE, MH, CT, GE, UD, BG. Supervision: CK, JM, UD, TM.

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Author notes

  1. J M Hönes and L Botezatu: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Hematology, West German Cancer Center, University Hospital Essen, University Duisburg-Essen, Essen, Germany

    J M Hönes, L Botezatu, L Vassen, S M Hergenhan, A Thivakaran, J Schütte, Y S Al-Matary, R F Lams, U Dührsen & C Khandanpour

  2. Institut de recherches cliniques de Montréal (IRCM), Hematopoiesis and Cancer Research Unit, and Mc Gill University, Montréal, Canada

    A Helness

  3. Institut de recherches cliniques de Montréal (IRCM), Hematopoiesis and Cancer Research Unit, and Université de Montréal, Montréal, Canada

    C Vadnais, J Fraszscak & T Möröy

  4. Institut de recherches cliniques de Montréal (IRCM), Chromatin and Genomic Expression Research Unit, and Université de Montréal, Montréal, Canada

    F Robert

  5. Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland, USA

    H Makishima, T Radivoyevitch, B Przychodzen & J P Maciejewski

  6. Institute for Transfusion Medicine, University Hospital Essen, University Duisburg-Essen, Essen, Germany

    S V da Conceição Castro, A Görgens & B Giebel

  7. CAPES Foundation, Ministry of Education of Brazil, Brasília, Brazil

    S V da Conceição Castro

  8. Institute for Cell Biology (Tumor Research), University Hospital Essen, University Duisburg-Essen, Germany

    L Klein-Hitpass & K Lennartz

  9. Department of Hematology, Hemostasis, Oncology, and Stem Cell Transplantation, Hannover Medical School, Hannover, Germany

    M Heuser

  10. Medical Clinic and Polyclinic, University Hospital Carl Gustav Carus, Technical University Dresden, Dresden, Germany

    C Thiede & G Ehninger

  11. Département de microbiologie, infectiologie et immunologie, Université de Montréal, Montréal, Canada

    T Möröy

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  1. J M Hönes
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  2. L Botezatu
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Corresponding authors

Correspondence to T Möröy or C Khandanpour.

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Competing interests

Cyrus Khandanpour received travel reimbursement for attending scientific conferences from Amgen and Chugai. Jaroslaw Maciejewski received speaker honoraria from Celgene and Alexion. The remaining authors declare no conflict of interest.

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Hönes, J., Botezatu, L., Helness, A. et al. GFI1 as a novel prognostic and therapeutic factor for AML/MDS. Leukemia 30, 1237–1245 (2016). https://doi.org/10.1038/leu.2016.11

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