bims-tremyl Biomed News
on Therapy resistance biology in myeloid leukemia
Issue of 2020–07–19
thirteen papers selected by
Paolo Gallipoli, Barts Cancer Institute, Queen Mary University of London



  1. J Clin Oncol. 2020 Jul 16. JCO1903345
       PURPOSE: Despite undergoing allogeneic hematopoietic stem cell transplantation (HCT), patients with acute myeloid leukemia (AML) with internal tandem duplication mutation in the FMS-like tyrosine kinase 3 gene (FLT3-ITD) have a poor prognosis, frequently relapse, and die as a result of AML. It is currently unknown whether a maintenance therapy using FLT3 inhibitors, such as the multitargeted tyrosine kinase inhibitor sorafenib, improves outcome after HCT.
    PATIENTS AND METHODS: In a randomized, placebo-controlled, double-blind phase II trial (SORMAIN; German Clinical Trials Register: DRKS00000591), 83 adult patients with FLT3-ITD-positive AML in complete hematologic remission after HCT were randomly assigned to receive for 24 months either the multitargeted and FLT3-kinase inhibitor sorafenib (n = 43) or placebo (n = 40 placebo). Relapse-free survival (RFS) was the primary endpoint of this trial. Relapse was defined as relapse or death, whatever occurred first.
    RESULTS: With a median follow-up of 41.8 months, the hazard ratio (HR) for relapse or death in the sorafenib group versus placebo group was 0.39 (95% CI, 0.18 to 0.85; log-rank P = .013). The 24-month RFS probability was 53.3% (95% CI, 0.36 to 0.68) with placebo versus 85.0% (95% CI, 0.70 to 0.93) with sorafenib (HR, 0.256; 95% CI, 0.10 to 0.65; log-rank P = .002). Exploratory data show that patients with undetectable minimal residual disease (MRD) before HCT and those with detectable MRD after HCT derive the strongest benefit from sorafenib.
    CONCLUSION: Sorafenib maintenance therapy reduces the risk of relapse and death after HCT for FLT3-ITD-positive AML.
    DOI:  https://doi.org/10.1200/JCO.19.03345
  2. Nat Commun. 2020 Jul 14. 11(1): 3506
      Acute myeloid leukemia (AML) is characterised by a series of genetic and epigenetic alterations that result in deregulation of transcriptional networks. One understudied source of transcriptional regulators are transposable elements (TEs), whose aberrant usage could contribute to oncogenic transcriptional circuits. However, the regulatory influence of TEs and their links to AML pathogenesis remain unexplored. Here we identify six endogenous retrovirus (ERV) families with AML-associated enhancer chromatin signatures that are enriched in binding of key regulators of hematopoiesis and AML pathogenesis. Using both locus-specific genetic editing and simultaneous epigenetic silencing of multiple ERVs, we demonstrate that ERV deregulation directly alters the expression of adjacent genes in AML. Strikingly, deletion or epigenetic silencing of an ERV-derived enhancer suppresses cell growth by inducing apoptosis in leukemia cell lines. This work reveals that ERVs are a previously unappreciated source of AML enhancers that may be exploited by cancer cells to help drive tumour heterogeneity and evolution.
    DOI:  https://doi.org/10.1038/s41467-020-17206-4
  3. Am J Hematol. 2020 Jul 18.
      Treatment of advanced-phase chronic myeloid leukemia (CML) remains unsatisfactory. Single-agent tyrosine kinase inhibitors have modest and short-lived activity in this setting. We conducted a phase I/II study to determine safety and efficacy of the combination of dasatinib and decitabine in patients with advanced CML. Two different dose schedules were investigated with a starting decitabine dose of either 10mg/m2 or 20mg/m2 daily for 10 days plus dasatinib 100 mg daily. The target dose level was decitabine 10mg/m2 or 20mg/m2 daily for 10 days plus dasatinib 140 mg daily. Thirty patients were enrolled, including 7 with accelerated-phase CML, 19 with blast-phase CML, and 4 with Philadelphia-chromosome positive acute myeloid leukemia. No dose-limiting toxicity was observed at the starting dose level with either schedule. Grade ≥3 treatment emergent hematological adverse events were reported in 28 patients. Thirteen patients (48%) achieved a major hematologic response and 6 (22%) achieved a minor hematologic response, with 44% of these patients achieving a major cytogenetic response and 33% achieving a major molecular response. Median overall survival (OS) was 13.8 months, with significantly higher OS among patients who achieved a hematologic response compared to non-responders (not reached versus 4.65 months; p<0.0001). Decitabine plus dasatinib is a safe and active regimen in advanced CML. Further studies using this combination are warranted. This article is protected by copyright. All rights reserved.
    DOI:  https://doi.org/10.1002/ajh.25939
  4. Leuk Res. 2020 Jul 02. pii: S0145-2126(20)30114-4. [Epub ahead of print]96 106409
      Acute myeloid leukemia (AML) is often characterized by the presence of specific and recurrent chromosomal abnormalities. Current treatments have greatly increased remission rate, but relapse still occurs. Therefore, novel therapeutic approaches are required. Previously, using a conditional Cbfb-MYH11 knockin mouse model, we showed that Cbfb-MYH11 induces the expression of a cytokine receptor, IL1RL1. Treatment with IL-33, the only known ligand of IL1RL1, promotes leukemia cell survival in vitro. We further found that IL1RL1+ cells survive better with chemotherapy than IL1RL1- population. However, the mechanism is not clear. Here, we show that IL-33 treatment decreased drug sensitivity in the human inv(16) AML cell line ME-1. By RT-PCR, we found that IL-33 increased the expression of IL-4 and IL-6 and led to the activation of both p38 MAPK and NF-κB. We also showed that IL-33 decreased apoptosis with increased phosphorylation of p38 MAPK. Moreover, pre-treatment with MAPK inhibitor attenuated the phosphorylation of p38 enhanced by IL-33 and reversed the anti-apoptotic effect by IL-33. Taken together, our findings give news insights into the potential mechanism of the anti-apoptotic effect by IL-33/IL1RL1 axis in AML which will help in future drug development.
    Keywords:  AML; IL-33; IL1RL1; p38 MAPK
    DOI:  https://doi.org/10.1016/j.leukres.2020.106409
  5. Leukemia. 2020 Jul 13.
      Classification of acute lymphoblastic and myeloid leukemias (ALL and AML) remains heavily based on phenotypic resemblance to normal hematopoietic precursors. This framework can provide diagnostic challenges for immunophenotypically heterogeneous immature leukemias, and ignores recent advances in understanding of developmental multipotency of diverse normal hematopoietic progenitor populations that are identified by transcriptional signatures. We performed transcriptional analyses of a large series of acute myeloid and lymphoid leukemias and detected significant overlap in gene expression between cases in different diagnostic categories. Bioinformatic classification of leukemias along a continuum of hematopoietic differentiation identified leukemias at the myeloid/T-lymphoid interface, which shared gene expression programs with a series of multi or oligopotent hematopoietic progenitor populations, including the most immature CD34+CD1a-CD7- subset of early thymic precursors. Within these interface acute leukemias (IALs), transcriptional resemblance to early lymphoid progenitor populations and biphenotypic leukemias was more evident in cases originally diagnosed as AML, rather than T-ALL. Further prognostic analyses revealed that expression of IAL transcriptional programs significantly correlated with poor outcome in independent AML patient cohorts. Our results suggest that traditional binary approaches to acute leukemia categorization are reductive, and that identification of IALs could allow better treatment allocation and evaluation of therapeutic options.
    DOI:  https://doi.org/10.1038/s41375-020-0965-z
  6. Haematologica. 2020 Jul 16. pii: haematol.2020.248807. [Epub ahead of print]
      Myelodysplastic syndromes (MDS) are hematological disorders at high risk of progression to secondary acute myeloid leukemia (sAML). However, the mutational dynamics and clonal evolution underlying disease progression are poorly understood at present. To elucidate the mutational dynamics of pathways and genes occurring during the evolution to sAML, next generation sequencing was performed on 84 serially paired samples of MDS patients who developed sAML (discovery cohort) and 14 paired samples from MDS patients who did not progress to sAML during follow-up (control cohort). Results were validated in an independent series of 388 MDS patients (validation cohort). We used an integrative analysis to identify how mutations, alone or in combination, contribute to leukemic transformation. The study showed that MDS progression to sAML is characterized by greater genomic instability and the presence of several types of mutational dynamics, highlighting increasing (STAG2) and newly-acquired (NRAS and FLT3) mutations. Moreover, we observed cooperation between genes involved in the cohesin and Ras pathways in 15-20% of MDS patients who evolved to sAML, as well as a high proportion of newly acquired or increasing mutations in the chromatin-modifier genes in MDS patients receiving a disease-modifying therapy before their progression to sAML.
    Keywords:  Myelodysplastic Syndromes; Next generation sequencing; Ras pathway; cohesin complex; sAML progression
    DOI:  https://doi.org/10.3324/haematol.2020.248807
  7. Cell Stem Cell. 2020 Jul 14. pii: S1934-5909(20)30285-X. [Epub ahead of print]
      DNA methyltransferase 3A (DNMT3A) is the most commonly mutated gene in clonal hematopoiesis (CH). Somatic DNMT3A mutations arise in hematopoietic stem cells (HSCs) many years before malignancies develop, but difficulties in comparing their impact before malignancy with wild-type cells have limited the understanding of their contributions to transformation. To circumvent this limitation, we derived normal and DNMT3A mutant lymphoblastoid cell lines from a germline mosaic individual in whom these cells co-existed for nearly 6 decades. Mutant cells dominated the blood system, but not other tissues. Deep sequencing revealed similar mutational burdens and signatures in normal and mutant clones, while epigenetic profiling uncovered the focal erosion of DNA methylation at oncogenic regulatory regions in mutant clones. These regions overlapped with those sensitive to DNMT3A loss after DNMT3A ablation in HSCs and in leukemia samples. These results suggest that DNMT3A maintains a conserved DNA methylation pattern, the erosion of which provides a distinct competitive advantage to hematopoietic cells.
    Keywords:  DNMT3A; HSC; cell competition; clonal hematopoiesis; hematopoietic stem cells; mutation burden; mutation signature
    DOI:  https://doi.org/10.1016/j.stem.2020.06.018
  8. J Chem Inf Model. 2020 Jul 17.
      FMS-like tyrosine kinase 3 (FLT3) is mutated in ~30% of patients that suffer from acute myeloid leukemia (AML). In about 25% of all AML patients, in-frame insertions are observed in the sequence. Most of those insertions are internal tandem duplications (ITDs) of a sequence from the protein. The characteristics of such mutations in terms of length, sequence and location were hitherto studied in different populations, but not in a comprehensive mutation database. Here, in-frame insertions into the FLT3 gene were extracted from the Catalogue of Somatic Mutations in Cancer (COSMIC) database. These were analyzed with respect to the length, location and sequence of the mutations. Furthermore, characteristic strings (sequences) of different lengths were identified. Mutations were shown to occur most often in the juxtamembrane zipper (JM-Z) domain of FLT3, followed by the hinge domain and first tyrosine kinase domain (TKD1), upstream of the phosphate-binding loop (P-loop). Interestingly, there are specific hot spot residues where insertions are more likely to occur. The insertions vary in length between one and 67 amino acids, with the largest insertions spanning the phosphate binding loop. Insertions that occur downstream of the P-loop are shorter. Our analysis further shows that acidic and aromatic residues are enriched in the insertions. Finally, molecular dynamics simulations were run for FLT3 with ITD insertions in the hinge and tyrosine kinase domains. Based on the findings, a mechanism is proposed for activation by ITDs, according to which there is no direct coupling between the length of the insertion and the activity of the mutated protein. The effect of insertions on the sensitivity of FLT3 to kinase inhibitors is discussed based on our findings.
    DOI:  https://doi.org/10.1021/acs.jcim.0c00544
  9. Blood Rev. 2020 Jun 03. pii: S0268-960X(20)30062-X. [Epub ahead of print] 100712
      Since the discovery of JAK2 V617F as a highly prevalent somatic acquired mutation in the majority of myeloproliferative neoplasms (MPNs), it has become clear that these diseases are driven by pathologic activation of JAK2 and eventually of STAT5 and other members of the STAT family. The concept was strengthened by the discovery of the other activating driver mutations in MPL (thrombopoietin receptor, TpoR) and in calreticulin gene, which all lead to persistent activation of wild type JAK2. Although with a rare frequency, MPNs can evolve to secondary acute myeloid leukemia (sAML), a condition that is resistant to treatment. Here we focus on the role of p53 in this transition. In sAML mutations in TP53 or amplification in genes coding for negative regulators of p53 are much more frequent than in de novo AML. We review studies that explore a signaling and biochemical interaction between activated STATs and p53 in MPNs and other cancers. With the development of advanced sequencing efforts, strong evidence has been presented for dominant negative effects of mutated p53 in leukemia. In other studies, gain of function effects have been described that might be cell type specific. A more profound understanding of the potential interaction between p53 and activated STATs is necessary in order to take full advantage of novel p53-targeted therapies.
    Keywords:  Myeloproliferative neoplasms; STATs; Transcription; p53 mutant; secondary acute myeloid leukemia
    DOI:  https://doi.org/10.1016/j.blre.2020.100712
  10. Cancer Discov. 2020 Jul 15. pii: CD-20-0026. [Epub ahead of print]
      We investigated the role of PRMT5 in MPN pathogenesis and aimed to elucidate key PRMT5 targets contributing to MPN maintenance. PRMT5 is overexpressed in primary MPN cells and PRMT5 inhibition potently reduced MPN cell proliferation ex vivo. PRMT5 inhibition was efficacious at reversing elevated hematocrit, leukocytosis and splenomegaly in a model of JAK2V617F+ polycythemia vera (PV) and leukocyte and platelet counts, hepatosplenomegaly and fibrosis in the MPLW515L model of myelofibrosis (MF). Dual targeting of JAK and PRMT5 was superior to JAK or PRMT5 inhibitor monotherapy, further decreasing elevated counts and extramedullary hematopoiesis in vivo. PRMT5 inhibition reduced expression of E2F targets and altered the methylation status of E2F1 leading to attenuated DNA damage repair, cell cycle arrest and increased apoptosis. Our data link PRMT5 to E2F1 regulatory function and MPN cell survival and provide a strong mechanistic rationale for clinical trials of PRMT5 inhibitors in MPN.
    DOI:  https://doi.org/10.1158/2159-8290.CD-20-0026