bims-tremyl Biomed News
on Therapy resistance biology in myeloid leukemia
Issue of 2023–06–18
forty papers selected by
Paolo Gallipoli, Barts Cancer Institute, Queen Mary University of London



  1. Trends Cancer. 2023 Jun 10. pii: S2405-8033(23)00095-X. [Epub ahead of print]
      Myeloid malignancies, a group of hematopoietic disorders that includes acute myeloid leukemia (AML), myelodysplastic syndromes (MDS), and myeloproliferative neoplasms (MPNs), are caused by the accumulation of genetic and epigenetic changes in hematopoietic stem and progenitor cells (HSPCs) over time. Despite the relatively low number of genomic drivers compared with other forms of cancer, the process by which these changes shape the genomic architecture of myeloid malignancies remains elusive. Recent advancements in clonal hematopoiesis research and the use of cutting-edge single cell technologies have shed new light on the developmental process of myeloid malignancies. In this review, we delve into the intricacies of clonal evolution in myeloid malignancies and its implications for the development of new diagnostic and therapeutic approaches.
    Keywords:  clonal evolution; mutation order; myeloid malignancies; single cell genomics
    DOI:  https://doi.org/10.1016/j.trecan.2023.05.004
  2. Am J Hematol. 2023 Jun 15.
      The nucleophosmin (NPM1) gene encodes for a multifunctional chaperone protein that is localized in the nucleolus but continuously shuttles between the nucleus and cytoplasm. NPM1 mutations occur in about one-third of AML, are AML-specific, usually involve exon 12 and are frequently associated with FLT3-ITD, DNMT3A, TET2, and IDH1/2 mutations. Because of its unique molecular and clinico-pathological features, NPM1-mutated AML is regarded as a distinct leukemia entity in both the International Consensus Classification (ICC) and the 5th edition of the World Health Organization (WHO) classification of myeloid neoplasms. All NPM1 mutations generate leukemic mutants that are aberrantly exported in the cytoplasm of the leukemic cells and are relevant to the pathogenesis of the disease. Here, we focus on recently identified functions of the NPM1 mutant at chromatin level and its relevance in driving HOX/MEIS gene expression. We also discuss yet controversial issues of the ICC/WHO classifications, including the biological and clinical significance of therapy-related NPM1-mutated AML and the relevance of blasts percentage in defining NPM1-mutated AML. Finally, we address the impact of new targeted therapies in NPM1-mutated AML with focus on CAR T cells directed against NPM1/HLA neoepitopes, as well as XPO1 and menin inhibitors.
    DOI:  https://doi.org/10.1002/ajh.26989
  3. Blood Adv. 2023 Jun 16. pii: bloodadvances.2022009468. [Epub ahead of print]
      Although allogeneic hematopoietic cell transplantation (allo-HCT) is curative for high-risk pediatric acute myeloid leukemia (AML), disease relapse remains the primary cause of post-transplant mortality. To identify pressures imposed by allo-HCT on AML cells that escape the graft-versus-leukemia effect, we evaluated immune signatures at diagnosis and post-transplant relapse in bone marrow samples from four pediatric patients using a multimodal single-cell proteogenomic approach. Downregulation of MHC class II expression was most profound in progenitor-like blasts and accompanied by correlative changes in transcriptional regulation. Dysfunction of activated NK cells and CD8+ T-cell subsets at relapse was evidenced by loss of response to IFN-γ, TNF-α signaling via NF-kβ, and IL-2/STAT5 signaling. Clonotype analysis of post-transplant relapse samples revealed expansion of dysfunctional T cells and enrichment of T-regulatory and T-helper cells. Using novel computational methods, our results illustrate a diverse immune-related transcriptional signature in post-transplant relapses not previously reported in pediatric AML.
    DOI:  https://doi.org/10.1182/bloodadvances.2022009468
  4. Leuk Lymphoma. 2023 Jun 16. 1-11
      The year 2023 marks the semi-centennial of the introduction of classic '7 + 3' chemotherapy for acute myeloid leukemia (AML) in 1973. It also marks the decennial of the first comprehensive sequencing efforts from The Cancer Genome Atlas (TCGA), which revealed that dozens of unique genes are recurrently mutated in AML genomes. Although more than 30 distinct genes have been implicated in AML pathogenesis, the current therapeutic armamentarium that is commercially available only targets FLT3 and IDH1/2 mutations, with olutasidenib as the most recent addition. This focused review spotlights management approaches that exploit the exquisite molecular dependencies of specific subsets of AML, with an emphasis on emerging therapies in the pipeline, including agents targeting TP53-mutant cells. We summarize precision and strategic targeting of AML based on leveraging functional dependencies and explore how mechanisms involving critical gene products can inform rational therapeutic design in 2024.
    Keywords:  Acute myeloid leukemia; TP53; metabolic vulnerabilities; mutational testing; targeted therapies
    DOI:  https://doi.org/10.1080/10428194.2023.2224473
  5. Hematology. 2023 Dec;28(1): 2223866
       OBJECTIVES: This study aimed to evaluate the incidence and prognostic significance of common cytogenetic and molecular abnormalities in patients with TP53-mutated and non-TP53-mutated acute myeloid leukemia (AML).
    METHODS: We retrospectively analyzed the clinical data of 326 patients with newly diagnosed AML hospitalized in our institution between October 2015 and June 2021. Classification variables were reported as percentages and compared by χ2 tests. Survival rates were evaluated by the Kaplan-Meier method.
    RESULTS: The incidence of TP53 mutations in AML patients in this clinic was 9.8%, of whom 87.5% patients were over 50 years old. The common concurrent mutations of TP53 were DNMT3A, IDH2, NRAS and TET2. Patients with a TP53 variant allele frequency (VAF) ≤ 40% had better overall survival (OS) than patients with a VAF >40%. Compared with non-TP53-mutated patients, significantly more TP53-mutated patients were gene-fusion negative, +mar, - 7/del (7q), - 5/del (5q), - 17/17p-, - 12/12p-, incomplete (inc) karyotype, or complex karyotype (CK), and had FLT3-ITD or IDH2 mutations, as well as a lower complete remission (CR) rate (31.3%) and higher recurrence rate (80.0%). The 2-year OS rates of TP53-mutated and non-TP53-mutated patients were 18.8% and 47.3%, respectively (P < 0.001). Univariate analysis showed that non-TP53-mutated patients with MLL family gene fusion, +mar or - 17/17p - karyotype, and FLT3-ITD mutations had a poor prognosis, while t(8; 21) karyotype was associated with a better prognosis. TP53-mutated patients with - 7/del (7q) or - 5/del (5q) karyotype had a poor prognosis.
    CONCLUSIONS: The cytogenetic and molecular landscapes differed between TP53-mutated and non-TP53-mutated patients, and some abnormalities had different values between them.
    Keywords:  Acute myeloid leukemia; cytogenetic abnormality; molecular abnormality; next-generation gene sequencing; prognosis
    DOI:  https://doi.org/10.1080/16078454.2023.2223866
  6. Clin Lymphoma Myeloma Leuk. 2023 May 23. pii: S2152-2650(23)00167-2. [Epub ahead of print]
       BACKGROUND: Dasatinib is a BCR::ABL1 tyrosine kinase inhibitor approved as frontline therapy at a 100 mg daily for chronic myeloid leukemia in chronic phase (CML-CP). The use of a lower dose of dasatinib (50 mg daily) has demonstrated better tolerance and improved outcomes compared with the standard dose. Here, we report the updated results in a large cohort with a 5-year follow-up.
    PATIENTS AND METHODS: Patients with newly diagnosed CML-CP were eligible. Entry and response-outcome criteria were standard. Dasatinib was given as 50 mg orally daily.
    RESULTS: Eighty-three patients were included. At 3 months, 78 (96%) patients achieved BCR::ABL1 transcripts (IS) ≤10%, and at 12 months, 65 (81%) patients achieved BCR::ABL1 transcript (IS) ≤0.1%. The cumulative incidence of complete cytogenetic, major molecular, and deep molecular responses at 5 years were 98%, 95%, and 82%, respectively. Rates of failures due to resistance (n = 4; 5%) and toxicity (n = 4; 5%) were low. The 5-year overall survival was 96% and event-free survival 90%. No transformations to accelerated or blastic phase were observed. Grade 3 to 4 pleural effusions developed in 2% of patients.
    CONCLUSION: Dasatinib 50 mg daily is an effective and safe treatment for newly diagnosed CML-CP.
    Keywords:  Complete cytogenetic response; Major molecular response; Outcome
    DOI:  https://doi.org/10.1016/j.clml.2023.05.009
  7. Cancer Res. 2023 Jun 16. pii: CAN-22-3682. [Epub ahead of print]
      Identifying mechanisms underlying relapse is a major clinical issue for effective cancer treatment. The emerging understanding of the importance of metastasis in hematological malignancies suggests that it could also play a role in drug resistance and relapse in acute myeloid leukemia (AML). In a cohort of 1,273 AML patients, we uncovered that the multifunctional scavenger receptor CD36 was positively associated with extramedullary dissemination of leukemic blasts, increased risk of relapse after intensive chemotherapy, and reduced event-free and overall survival. CD36 was dispensable for lipid uptake but fostered blast migration through its binding with thrombospondin-1. CD36-expressing blasts, which were largely enriched after chemotherapy, exhibited a senescent-like phenotype while maintaining their migratory ability. In xenograft mouse models, CD36 inhibition reduced metastasis of blasts and prolonged survival of chemotherapy-treated mice. These results pave the way for the development of CD36 as an independent marker of poor prognosis in AML patients and a promising actionable target to improve the outcome of patients.
    DOI:  https://doi.org/10.1158/0008-5472.CAN-22-3682
  8. Hemasphere. 2023 Jun;7(6): e914
      Acute myeloid leukemia (AML) is the most aggressive adult leukemia, characterized by clonal differentiation arrest of progenitor or precursor hematopoietic cells. Intense preclinical and clinical research has led to regulatory approval of several targeted therapeutics, administered either as single agents or as combination therapies. However, the majority of patients still face a poor prognosis and disease relapse frequently occurs due to selection of therapy-resistant clones. Hence, more effective novel therapies, most likely as innovative, rational combination therapies, are urgently needed. Chromosomal aberrations, gene mutations, and epigenetic alterations drive AML pathogenesis but concurrently provide vulnerabilities to specifically target leukemic cells. Other molecules, either aberrantly active and/or overexpressed in leukemic stem cells, may also be leveraged for therapeutic benefit. This concise review of targeted therapies for AML treatment, which are either approved or are being actively investigated in clinical trials or recent preclinical studies, provides a flavor of the direction of travel, but also highlights the current challenges in AML treatment.
    DOI:  https://doi.org/10.1097/HS9.0000000000000914
  9. Genes Chromosomes Cancer. 2023 Jun 12.
      Germline RUNX1 mutations lead to familial platelet disorder with associated myeloid malignancy (FPDMM), characterized by thrombocytopenia, abnormal bleeding, and an elevated risk of developing myelodysplastic neoplasia (MDS) and acute myeloid leukemia (AML) at young age. However, it is not known why or how germline carriers of RUNX1 mutations have a particular propensity to develop myeloid hematologic malignancies, but the acquisition and composition of somatic mutations are believed to initiate and determine disease progression. We present a novel family pedigree that shares a common germline RUNX1R204* variant and exhibits a spectrum of somatic mutations and related myeloid malignancies (MM). RUNX1 mutations are associated with inferior clinical outcome; however, the proband of this family developed MDS with ring sideroblasts (MDS-RS), classified as a low-risk MDS subgroup. His relatively indolent clinical course is likely due to a specific somatic mutation in the SF3B1 gene. While the three main RUNX1 isoforms have been ascribed various roles in normal hematopoiesis, they are now being increasingly recognized as involved in myeloid disease. We investigated the RUNX1 transcript isoform patterns in the proband and his sister, who carries the same germline RUNX1R204* variant, and has FPDMM but no MM. We demonstrate a RUNX1a increase in MDS-RS, as previously reported in MM. Interestingly, we identify a striking unbalance of RUNX1b and -c in FPDMM. In conclusion, this report reinforces the relevance of somatic variants on the clinical phenotypic heterogeneity in families with germline RUNX1 deficiency and investigates a potential new role for RUNX1 isoform disequilibrium as a mechanism for development of MM.
    Keywords:  FPDMM; MDS; RUNX1; RUNX1 isoforms; germline mutations; myeloid malignancies
    DOI:  https://doi.org/10.1002/gcc.23184
  10. Blood Adv. 2023 Jun 16. pii: bloodadvances.2023010173. [Epub ahead of print]
      The increasing knowledge of molecular genetics of acute myeloid leukemia (AML) urged the update of previous diagnostic and prognostic schemes, which resulted in the development, in 2022, of the World Health Organization (WHO), the International Consensus Classification (ICC) and the new European LeukemiaNet (ELN) recommendations. We aimed to provide a real-world application of the new models, to unravel differences and similarities, and to test their implementation in clinical AML diagnosis. A total of 1001 patients diagnosed with AML were re-classified according to the new schemes. The overall diagnostic changes between the WHO 2016, compared to WHO 2022 and ICC classifications were 22.8% and 23.7%, respectively, with a 13.1% difference in patients' distribution between ICC and WHO 2022. The 2022 ICC "not otherwise specified" and WHO "defined by differentiation" AML categories shrank as compared to WHO 2016 (24.1% and 26.8% respectively, vs 38.7%), particularly due to an expansion of the myelodysplasia (MDS)-related group. Of 397 patients with a MDS-related AML according to the ICC, 55.9% were defined by the presence of a MDS-related karyotype. The overall re-stratification between ELN 2017 and 2022 was 12.9%. The 2022 AML classifications led to a significant improvement of diagnostic schemes. In the real-world setting, conventional cytogenetics, usually rapidly available and less expensive than molecular characterization, stratified 56% of secondary AML, still maintaining a powerful diagnostic role. Considering the similarities between WHO and ICC diagnostic schemes, a tentative to generate a unified model is desirable.
    DOI:  https://doi.org/10.1182/bloodadvances.2023010173
  11. J Clin Invest. 2023 06 15. pii: e165510. [Epub ahead of print]133(12):
      RAS mutations are among the most prevalent oncogenic drivers in cancers. RAS proteins propagate signals only when associated with cellular membranes as a consequence of lipid modifications that impact their trafficking. Here, we discovered that RAB27B, a RAB family small GTPase, controlled NRAS palmitoylation and trafficking to the plasma membrane, a localization required for activation. Our proteomic studies revealed RAB27B upregulation in CBL- or JAK2-mutated myeloid malignancies, and its expression correlated with poor prognosis in acute myeloid leukemias (AMLs). RAB27B depletion inhibited the growth of CBL-deficient or NRAS-mutant cell lines. Strikingly, Rab27b deficiency in mice abrogated mutant but not WT NRAS-mediated progenitor cell growth, ERK signaling, and NRAS palmitoylation. Further, Rab27b deficiency significantly reduced myelomonocytic leukemia development in vivo. Mechanistically, RAB27B interacted with ZDHHC9, a palmitoyl acyltransferase that modifies NRAS. By regulating palmitoylation, RAB27B controlled c-RAF/MEK/ERK signaling and affected leukemia development. Importantly, RAB27B depletion in primary human AMLs inhibited oncogenic NRAS signaling and leukemic growth. We further revealed a significant correlation between RAB27B expression and sensitivity to MEK inhibitors in AMLs. Thus, our studies presented a link between RAB proteins and fundamental aspects of RAS posttranslational modification and trafficking, highlighting future therapeutic strategies for RAS-driven cancers.
    Keywords:  Cancer; Cell Biology; Hematology; Signal transduction
    DOI:  https://doi.org/10.1172/JCI165510
  12. Cancers (Basel). 2023 May 30. pii: 2991. [Epub ahead of print]15(11):
      Mutations of the FLT3 gene are among the most common genetic aberrations detected in AML and occur mainly as internal tandem duplications (FLT3-ITD). However, the specific sites of FLT3-ITD insertion within FLT3 show marked heterogeneity regarding both biological and clinical features. In contrast to the common assumption that ITD insertion sites (IS) are restricted to the juxtamembrane domain (JMD) of FLT3, 30% of FLT3-ITD mutations insert at the non-JMD level, thereby integrating into various segments of the tyrosine kinase subdomain 1 (TKD1). ITDs inserted within TKD1 have been shown to be associated with inferior complete remission rates as well as shorter relapse-free and overall survival. Furthermore, resistance to chemotherapy and tyrosine kinase inhibition (TKI) is linked to non-JMD IS. Although FLT3-ITD mutations in general are already recognized as a negative prognostic marker in currently used risk stratification guidelines, the even worse prognostic impact of non-JMD-inserting FLT3-ITD has not yet been particularly considered. Recently, the molecular and biological assessment of TKI resistance highlighted the pivotal role of activated WEE1 kinase in non-JMD-inserting ITDs. Overcoming therapy resistance in non-JMD FLT3-ITD-mutated AML may lead to more effective genotype- and patient-specific treatment approaches.
    Keywords:  FLT3 mutation; acute myeloid leukemia (AML); chemotherapy resistance; internal tandem duplications (FLT3-ITD); non-juxtamembrane domain (non-JMD) insertion site; tyrosine kinase inhibition (TKI)
    DOI:  https://doi.org/10.3390/cancers15112991
  13. J Clin Med. 2023 May 24. pii: 3647. [Epub ahead of print]12(11):
      The traditionally dismal outcome of acute myeloid leukemia (AML) patients carrying the FMS-related tyrosine kinase 3 (FLT3) mutations has been mitigated by the recent introduction of tyrosine kinase inhibitors (TKI) into clinics, such as midostaurin and gilteritinib. The present work summarizes the clinical data that led to the use of gilteritinib in clinical practice. Gilteritinib is a second-generation TKI with deeper single-agent activity than first-generation drugs against both FLT3-ITD and TKD mutations in human studies. Moreover, the phase I/II dose-escalation, dose-expansion Chrysalis trial showed an acceptable safety profile of gilteritinib (diarrhea, elevated aspartate aminotransferase, febrile neutropenia, anemia, thrombocytopenia, sepsis, and pneumonia) and a 49% overall response rate (ORR) in 191 FLT3-mutated relapsed/refractory (R/R) AML patients. In 2019, the pivotal ADMIRAL trial showed that the median overall survival was significantly longer in patients treated with gilteritinib than among those receiving chemotherapy (9.3 vs. 5.6 months, respectively) and the ORR to gilteritinib was 67.6%, outperforming the 25.8% for chemotherapy arm and leading to the license for its clinical use by the US Food and Drug Administration. Since then, several real-world experiences have confirmed the positive results in the R/R AML setting. Finally, gilteritinib-based combinations currently under investigation, with several compounds (venetoclax, azacitidine, conventional chemotherapy, etc.) and some practical tips (maintenance after allogeneic transplantation, interaction with antifungal drugs, extramedullary disease, and onset of resistance), will be analyzed in detail in this review.
    Keywords:  FLT3 mutations; gilteritinib; resistant/relapsed acute myeloid leukemia; tyrosine kinase inhibitors
    DOI:  https://doi.org/10.3390/jcm12113647
  14. Exp Hematol. 2023 Jun 07. pii: S0301-472X(23)00252-7. [Epub ahead of print]
      Recent studies have uncovered similarities and differences between two highly homologous epigenetic reading proteins, ENL (MLLT1) and AF9 (MLLT3) with therapeutic implications. The importance of these proteins has traditionally been exemplified by their involvement in chromosomal translocations with the Mixed Lineage Leukemia gene (MLL; aka KMT2a). MLL-rearrangements occur in a subset of acute leukemias and generate potent oncogenic MLL-fusion proteins that impact epigenetic and transcriptional regulation. Leukemic patients with MLL-rearrangements display intermediate to poor prognoses, necessitating further mechanistic research. Several protein complexes involved in regulating RNA polymerase II transcription and the epigenetic landscape are hijacked in MLL-r leukemia that include ENL and AF9. Recent biochemical studies have defined a highly homologous YEATS domain in ENL and AF9 that binds acylated histones, which aids in the localization and retention of these proteins to transcriptional targets. In addition, detailed characterization of the homologous AHD on ENL and AF9 have revealed differential association with transcriptional activating and repressing complexes. Importantly, CRISPR knock out screens have demonstrated a unique role for wild type ENL in leukemic stem cell function, whereas AF9 appears important for normal hematopoietic stem cells. In this perspective, we examine the ENL and AF9 proteins with attention to recent work characterizing the epigenetic reading YEATS domains and AHD on both the wild type proteins and when fused to MLL. We summarize drug development efforts and their therapeutic potential and assess ongoing research that has refined our understanding of how these proteins function, which continues to reveal new therapeutic avenues.
    Keywords:  AF9 (MLLT3); Anc1 Homology Domain (AHD); DOT1L; ENL (MLLT1); MLL (KMT2a); SEC; YEATS
    DOI:  https://doi.org/10.1016/j.exphem.2023.06.001
  15. Am Soc Clin Oncol Educ Book. 2023 Jun;43 e390010
      In this review, we discuss the use of measurable residual disease (MRD) in AML, ALL, and chronic myeloid leukemia (CML). Our aims were to review the different methodologies for MRD assessment; describe the clinical relevance and medical decision making on the basis of MRD; compare and contrast the usage of MRD across AML, ALL, and CML; and discuss what patients need to know about MRD as it relates to their disease status and treatment. Finally, we discuss ongoing challenges and future directions with the goal of optimizing MRD usage in leukemia management.
    DOI:  https://doi.org/10.1200/EDBK_390010
  16. Blood Adv. 2023 Jun 14. pii: bloodadvances.2023009885. [Epub ahead of print]
      Late acute GVHD is defined as de novo acute GVHD presenting beyond 100 days after allogeneic hematopoietic cell transplantation (HCT) without manifestations of chronic GVHD. Data are limited regarding its characteristics, clinical course, and risk factors due to under recognition and changes in classification. We evaluated 3542 consecutive adult recipients of their first HCT at twenty-four Mount Sinai Acute GVHD International Consortium (MAGIC) centers between January 2014 and August 2021 to better describe the clinical evolution and outcomes of late acute GVHD. The cumulative incidence of classic acute GVHD that required systemic treatment was 35.2% and an additional 5.7% of patients required treatment for late acute GVHD. At the onset of symptoms, late acute GVHD was more severe than classic acute GVHD by both clinical and MAGIC Algorithm Probability (MAP) biomarker parameters, and showed a lower overall response rate at day 28. Both clinical and biomarker grading at the time of treatment stratified the risk of NRM in patients with classic and late acute GVHD, respectively, but long-term NRM and OS did not differ between patients with classic and late acute GVHD. Advanced age, female to male sex mismatch, and the use of reduced intensity conditioning were associated with development of late acute GVHD, whereas use of post-transplant cyclophosphamide-based GVHD prevention was protective mainly due to shifts in GVHD timing. As overall outcomes were comparable, our findings, while not definitive, suggest that similar treatment strategies, including eligibility for clinical trials, based solely on clinical presentation at onset are appropriate.
    DOI:  https://doi.org/10.1182/bloodadvances.2023009885
  17. Lancet. 2023 Jun 09. pii: S0140-6736(23)00874-7. [Epub ahead of print]
       BACKGROUND: Erythropoiesis-stimulating agents (ESAs) are the standard-of-care treatment for anaemia in most patients with lower-risk myelodysplastic syndromes but responses are limited and transient. Luspatercept promotes late-stage erythroid maturation and has shown durable clinical efficacy in patients with lower-risk myelodysplastic syndromes. In this study, we report the results of a prespecified interim analysis of luspatercept versus epoetin alfa for the treatment of anaemia due to lower-risk myelodysplastic syndromes in the phase 3 COMMANDS trial.
    METHODS: The phase 3, open-label, randomised controlled COMMANDS trial is being conducted at 142 sites in 26 countries. Eligible patients were aged 18 years or older, had a diagnosis of myelodysplastic syndromes of very low risk, low risk, or intermediate risk (per the Revised International Prognostic Scoring System), were ESA-naive, and required red blood cell transfusions (2-6 packed red blood cell units per 8 weeks for ≥8 weeks immediately before randomisation). Integrated response technology was used to randomly assign patients (1:1, block size 4) to luspatercept or epoetin alfa, stratified by baseline red blood cell transfusion burden (<4 units per 8 weeks vs ≥4 units per 8 weeks), endogenous serum erythropoietin concentration (≤200 U/L vs >200 to <500 U/L), and ring sideroblast status (positive vs negative). Luspatercept was administered subcutaneously once every 3 weeks starting at 1·0 mg/kg body weight with possible titration up to 1·75 mg/kg. Epoetin alfa was administered subcutaneously once a week starting at 450 IU/kg body weight with possible titration up to 1050 IU/kg (maximum permitted total dose of 80 000 IU). The primary endpoint was red blood cell transfusion independence for at least 12 weeks with a concurrent mean haemoglobin increase of at least 1·5 g/dL (weeks 1-24), assessed in the intention-to-treat population. Safety was assessed in patients who received at least one dose of study treatment. The COMMANDS trial was registered with ClinicalTrials.gov, NCT03682536 (active, not recruiting).
    FINDINGS: Between Jan 2, 2019 and Aug 31, 2022, 356 patients were randomly assigned to receive luspatercept (178 patients) or epoetin alfa (178 patients), comprising 198 (56%) men and 158 (44%) women (median age 74 years [IQR 69-80]). The interim efficacy analysis was done for 301 patients (147 in the luspatercept group and 154 in the epoetin alfa group) who completed 24 weeks of treatment or discontinued earlier. 86 (59%) of 147 patients in the luspatercept group and 48 (31%) of 154 patients in the epoetin alfa group reached the primary endpoint (common risk difference on response rate 26·6; 95% CI 15·8-37·4; p<0·0001). Median treatment exposure was longer for patients receiving luspatercept (42 weeks [IQR 20-73]) versus epoetin alfa (27 weeks [19-55]). The most frequently reported grade 3 or 4 treatment-emergent adverse events with luspatercept (≥3% patients) were hypertension, anaemia, dyspnoea, neutropenia, thrombocytopenia, pneumonia, COVID-19, myelodysplastic syndromes, and syncope; and with epoetin alfa were anaemia, pneumonia, neutropenia, hypertension, iron overload, COVID-19 pneumonia, and myelodysplastic syndromes. The most common suspected treatment-related adverse events in the luspatercept group (≥3% patients, with the most common event occurring in 5% patients) were fatigue, asthenia, nausea, dyspnoea, hypertension, and headache; and none (≥3% patients) in the epoetin alfa group. One death after diagnosis of acute myeloid leukaemia was considered to be related to luspatercept treatment (44 days on treatment).
    INTERPRETATION: In this interim analysis, luspatercept improved the rate at which red blood cell transfusion independence and increased haemoglobin were achieved compared with epoetin alfa in ESA-naive patients with lower-risk myelodysplastic syndromes. Long-term follow-up and additional data will be needed to confirm these results and further refine findings in other subgroups of patients with lower-risk myelodysplastic syndromes, including non-mutated SF3B1 or ring sideroblast-negative subgroups.
    FUNDING: Celgene and Acceleron Pharma.
    DOI:  https://doi.org/10.1016/S0140-6736(23)00874-7
  18. Br J Haematol. 2023 Jun 12.
      Limited data exist on COVID-19 vaccination efficacy in patients with acute myeloid leukemia and myelodysplasia with excess blasts (AML/MDS-EB2). We report results from a prospective study, PACE (Patients with AML and COVID-19 Epidemiology). 93 patients provided samples post-vaccine 2 or 3 (PV2, PV3). Antibodies against SARS-COV-2 spike antigen were detectable in all samples. Neutralization of the omicron variant was poorer than ancestral variants but improved PV3. In contrast, adequate T-cell reactivity to SARS-COV-2 spike protein was seen in only 16/47 (34%) patients PV2 and 23/52 (44%) PV3. Using regression models, disease response (not in CR/Cri), and increasing age predicted poor T cell response.
    Keywords:  AML; COVID; MDS; vaccination
    DOI:  https://doi.org/10.1111/bjh.18894
  19. Haematologica. 2023 Jun 15.
      Certain subtypes of acute myeloid leukemia (AML) in children have inferior outcome, such as AML with translocation t(7;12)(q36;p13) leading to a MNX1::ETV6 fusion along with high expression of MNX1. We have identified the transforming event in this AML and possible ways of treatment. Retroviral expression of MNX1 was able to induce AML in mice, with similar gene expression and pathway enrichment to t(7;12) AML patient data. Importantly, this leukemia was only induced in immune incompetent mice using fetal but not adult hematopoietic stem and progenitor cells. The restriction in transforming capacity to cells from fetal liver is in alignment with t(7;12)(q36;p13) AML being mostly seen in infants. Expression of MNX1 led to increased histone 3 lysine 4 mono-, di- and trimethylation, reduction in H3K27me3, accompanied with changes in genome-wide chromatin accessibility and genome expression, likely mediated through MNX1 interaction with the methionine cycle and methyltransferases. MNX1 expression increased DNA damage, depletion of the Lin- /Sca1+/c-Kit+ population and skewing toward the myeloid lineage. These effects, together with leukemia development, was prevented by pretreatment with the S-adenosylmethionine analog Sinefungin. In conclusion, we have shown the importance of MNX1 in development of AML with t(7;12), supporting a rationale for targeting MNX1 and downstream pathways.
    DOI:  https://doi.org/10.3324/haematol.2022.282255
  20. Am Soc Clin Oncol Educ Book. 2023 Jun;43 e390026
      Myeloid malignancies are a manifestation of clonal expansion of hematopoietic cells driven by somatic genetic alterations that may arise in a potential background of deleterious germline variants. As next-generation sequencing technology has become more accessible, real-world experience has allowed integration of molecular genomic data with morphology, immunophenotype, and conventional cytogenetics to refine our understanding of myeloid malignancies. This has prompted revisions in the classification and the prognostication schema of myeloid malignancies and germline predisposition to hematologic malignancies. This review provides an overview of significant changes in the recently published classifications of AML and myelodysplastic syndrome, emerging prognostic scoring, and the role of germline deleterious variants in predisposing to MDS and AML.
    DOI:  https://doi.org/10.1200/EDBK_390026
  21. Br J Pharmacol. 2023 Jun 13.
      Although chemotherapeutic regimens can eliminate blasts in leukemia patients, they are associated with toxicity and often fail to eliminate all malignant cells resulting in disease relapse. Disease relapse has been attributed to the persistence of leukemia cells in the bone marrow (BM) with the capacity to recapitulate disease, these cells are often referred to as leukemia stem cells (LSCs). While LSCs have distinct characteristics in terms of pathobiology and immunophenotype, they are regulated by their interactions with the surrounding microenvironment. Thus, understanding the interaction between LSCs and their microenvironment is critical to identify effective therapies. To this end, there are numerous efforts to develop models to study such interactions. In this review, we will focus on the reciprocal interactions between LSCs and their milieu in the BM. Furthermore, we will highlight relevant therapies targeting these interactions and discuss some of the promising in vitro models designed to mimic such relationship.
    Keywords:  bone marrow; in vitro leukemia models; leukemia; leukemia stem cells; microenvironment
    DOI:  https://doi.org/10.1111/bph.16162
  22. Blood. 2023 Jun 10. pii: blood.2023020578. [Epub ahead of print]
      Hematological toxicity represents the most common adverse event following chimeric antigen receptor (CAR) T-cell therapy. Cytopenias can be profound, long-lasting, and can predispose for severe infectious complications. In a recent worldwide survey, we demonstrated that there remains considerable heterogeneity in regards to current practice patterns. Here, we sought to build consensus on the grading and management of Immune Effector Cell Associated Hemato-Toxicity (ICAHT) following CAR-T therapy. For this purpose, a joint effort between the European society for Blood and Marrow Transplantation (EBMT) and the European Hematology Association (EHA) involved an international panel of 36 CAR-T experts who met in a series of virtual conferences, culminating in a 2-day meeting in Lille, France. On the basis of these deliberations, best practice recommendations were developed. For the grading of ICAHT, a classification system based on depth and duration of neutropenia was developed for early (day 0-30) and late cytopenia (after day +30). Detailed recommendations on risk factors, available pre-infusion scoring systems (e.g. CAR-HEMATOTOX score), and diagnostic work-up are provided. A further section focuses on identifying hemophagocytosis in the context of severe hematotoxicity. Finally, we review current evidence and provide consensus recommendations for the management of ICAHT, including growth factor support, anti-infectious prophylaxis, transfusions, autologous hematopoietic cell boost, and allogeneic hematopoietic cell transplantation. In conclusion, we propose ICAHT as a novel toxicity category following immune effector cell therapy, provide a framework for its grading, review literature on risk factors, and outline expert recommendations for the diagnostic work-up and short- and long-term management.
    DOI:  https://doi.org/10.1182/blood.2023020578
  23. Commun Biol. 2023 Jun 09. 6(1): 622
      Acute myeloid leukemia is the most common acute leukemia in adults, the barrier of refractory and drug resistance has yet to be conquered in the clinical. Abnormal gene expression and epigenetic changes play an important role in pathogenesis and treatment. A super-enhancer is an epigenetic modifier that promotes pro-tumor genes and drug resistance by activating oncogene transcription. Multi-omics integrative analysis identifies the super-enhancer-associated gene CAPG and its high expression level was correlated with poor prognosis in AML. CAPG is a cytoskeleton protein but has an unclear function in AML. Here we show the molecular function of CAPG in regulating NF-κB signaling pathway by proteomic and epigenomic analysis. Knockdown of Capg in the AML murine model resulted in exhausted AML cells and prolonged survival of AML mice. In conclusion, SEs-associated gene CAPG can contributes to AML progression through NF-κB.
    DOI:  https://doi.org/10.1038/s42003-023-04973-1
  24. Blood Adv. 2023 Jun 16. pii: bloodadvances.2023010407. [Epub ahead of print]
      Peripheral blood stem cells are the most common source of hematopoietic stem and progenitor cells (HSPCs) used for hematopoietic cell transplantation (HCT). HSPC mobilization with G-CSF +/- plerixafor results in suboptimal HSPC yields in up to 30% of patients, despite multiple injections and leukapheresis procedures (LP). We evaluated motixafortide (BL-8040), a high-affinity, long-acting CXCR4 inhibitor with rapid mobilizing kinetics, in a multi-center, open-label, single-arm, 2-part, Phase II study to mobilize HSPCs in allogeneic HCT donors (NCT02639559). The primary endpoint was the efficacy of 1 dose of motixafortide to mobilize greater than or equal to 2.0×10^6 CD34+ cells/kg within 2 LPs. Twenty-five donor-recipient pairs were enrolled. Motixafortide was well-tolerated with 22/24 (92%) evaluable donors meeting the primary endpoint, including 11/11 donors receiving motixafortide at 1.25mg/kg. Engraftment and GVHD rates were comparable to historical data. Motixafortide preferentially mobilized large numbers of multipotent HSPCs and a smaller proportion of CD34+ plasmacytoid dendritic cell precursors with high CD123 expression. Motixafortide induced pan-mobilization of all major myeloid and lymphoid subsets, with maximum relative changes in plasmacytoid/myeloid dendritic cells, B-cells, basophils, CD8 T-cells and classical monocytes. In conclusion, a single injection of motixafortide results in rapid and sustained mobilization of multipotent HSPCs for allogeneic HCT.
    DOI:  https://doi.org/10.1182/bloodadvances.2023010407
  25. Nat Med. 2023 Jun 15.
    NHLBI Trans-Omics for Precision Medicine (TOPMed) Consortium
      Clonal hematopoiesis of indeterminate potential (CHIP) is a premalignant expansion of mutated hematopoietic stem cells. As CHIP-associated mutations are known to alter the development and function of myeloid cells, we hypothesized that CHIP may also be associated with the risk of Alzheimer's disease (AD), a disease in which brain-resident myeloid cells are thought to have a major role. To perform association tests between CHIP and AD dementia, we analyzed blood DNA sequencing data from 1,362 individuals with AD and 4,368 individuals without AD. Individuals with CHIP had a lower risk of AD dementia (meta-analysis odds ratio (OR) = 0.64, P = 3.8 × 10-5), and Mendelian randomization analyses supported a potential causal association. We observed that the same mutations found in blood were also detected in microglia-enriched fraction of the brain in seven of eight CHIP carriers. Single-nucleus chromatin accessibility profiling of brain-derived nuclei in six CHIP carriers revealed that the mutated cells comprised a large proportion of the microglial pool in the samples examined. While additional studies are required to validate the mechanistic findings, these results suggest that CHIP may have a role in attenuating the risk of AD.
    DOI:  https://doi.org/10.1038/s41591-023-02397-2
  26. Blood. 2023 Jun 15. pii: blood.2022019537. [Epub ahead of print]
      The bone marrow microenvironment (BMM) can regulate leukemia stem cells (LSC) via secreted factors. Increasing evidence suggests that dissecting the mechanisms by which BMM maintains LSC may lead to the development of effective therapies for the eradication of leukemia. Inhibitor of DNA binding 1 (ID1), a key transcriptional regulator in LSC previously identified by us, controls cytokine production in the BMM, but the role of ID1 in AML-BMM remains obscure. Here, we report that ID1 is highly expressed in the BMM of AML patients, especially in bone marrow mesenchymal stem cells (BMSCs), and the high expression of ID1 in AML-BMM is induced by BMP6, secreted from AML cells. Knocking out ID1 in mesenchymal cells significantly suppresses the proliferation of co-cultured AML cells. Loss of Id1 in BMM results in impaired AML progression in AML mouse models. Mechanistically, we found that Id1 deficiency significantly reduces SP1 protein levels in mesenchymal cells co-cultured with AML cells. Using ID1-interactome analysis, we found that ID1 interacts with RNF4, an E3 ubiquitin ligase, and causes a decrease in SP1 ubiquitination. Disrupting the ID1-RNF4 interaction by truncation in mesenchymal cells significantly reduces SP1 protein levels and delays AML cell proliferation. We identify that the target of Sp1, Angptl7, is the primary differentially expression protein factor in Id1 deficient bone marrow supernatant fluid (BMSF) to regulate AML progression in mice. Taken together, our study highlights the critical role of ID1 in AML-BMM and aids the development of therapeutic strategies for AML.
    DOI:  https://doi.org/10.1182/blood.2022019537
  27. iScience. 2023 Jun 16. 26(6): 106962
      DHX9 is a member of the DEAH (Asp-Glu-Ala-His) helicase family and regulates DNA replication and RNA processing. DHX9 dysfunction promotes tumorigenesis in several solid cancers. However, the role of DHX9 in MDS is still unknown. Here, we analyzed the expression of DHX9 and its clinical significance in 120 MDS patients and 42 non-MDS controls. Lentivirus-mediated DHX9-knockdown experiments were performed to investigate its biological function. We also performed cell functional assays, gene microarray, and pharmacological intervention to investigate the mechanistic involvement of DHX9. We found that overexpression of DHX9 is frequent in MDS and associated with poor survival and high risk of acute myeloid leukemia (AML) transformation. DHX9 is essential for the maintenance of malignant proliferation of leukemia cells, and DHX9 suppression increases cell apoptosis and causes hypersensitivity to chemotherapeutic agents. Besides, knockdown of DHX9 inactivates the PI3K-AKT and ATR-Chk1 signaling, promotes R-loop accumulation, and R-loop-mediated DNA damage.
    Keywords:  Cancer; Medical Microbiology; Pathophysiology
    DOI:  https://doi.org/10.1016/j.isci.2023.106962
  28. Blood Adv. 2023 Jun 14. pii: bloodadvances.2022008939. [Epub ahead of print]
      Impaired protein homeostasis, though well established in age-related disorders, has been linked in recent research with the pathogenesis of myeloproliferative neoplasms (MPNs). As yet, however, little is known about MPN-specific modulators of proteostasis, thus impeding our ability for increased mechanistic understanding and discovery of additional therapeutic targets. Loss of proteostasis, in itself, is traced to dysregulated mechanisms in protein folding and intracellular calcium signaling at the endoplasmic reticulum (ER). Here, using ex vivo and in vitro systems (including CD34+ cultures from patient bone marrow, and healthy cord/peripheral blood specimens), we extend our prior data from MPN patient platelet RNA sequencing, and discover select proteostasis-associated markers at RNA and/or protein levels in each of platelets, parent megakaryocytes, and whole blood specimens. Importantly, we identify a novel role in MPNs for enkurin (ENKUR), a calcium mediator protein, implicated originally only in spermatogenesis. Our data reveal consistent ENKUR downregulation at both RNA and protein levels across MPN patient specimens and experimental models, with a concomitant upregulation of a cell cycle marker, CDC20. Silencing of ENKUR by shRNA in CD34+ derived megakaryocytes further confirm this association with CDC20 at both RNA and protein levels; and indicate a likely role for the PI3K/Akt pathway. The inverse association of ENKUR and CDC20 expression was further confirmed upon treatment with thapsigargin (an agent that causes protein misfolding in the ER by selective loss of calcium) in both megakaryocyte and platelet fractions at RNA and protein levels. Together, our work sheds light on enkurin as a novel marker of MPN pathogenesis beyond the genetic alterations; and indicates further mechanistic investigation into a role for dysregulated calcium homeostasis, and ER and protein folding stress in MPN transformation.
    DOI:  https://doi.org/10.1182/bloodadvances.2022008939
  29. Hemasphere. 2023 Jun;7(6): e895
      Specific cell types and, therefore, organs respond differently during aging. This is also true for the hematopoietic system, where it has been demonstrated that hematopoietic stem cells alter a variety of features, such as their metabolism, and accumulate DNA damage, which can lead to clonal outgrowth over time. In addition, profound changes in the bone marrow microenvironment upon aging lead to senescence in certain cell types such as mesenchymal stem cells and result in increased inflammation. This heterogeneity makes it difficult to pinpoint the molecular drivers of organismal aging gained from bulk approaches, such as RNA sequencing. A better understanding of the heterogeneity underlying the aging process in the hematopoietic compartment is, therefore, needed. With the advances of single-cell technologies in recent years, it is now possible to address fundamental questions of aging. In this review, we discuss how single-cell approaches can and indeed are already being used to understand changes observed during aging in the hematopoietic compartment. We will touch on established and novel methods for flow cytometric detection, single-cell culture approaches, and single-cell omics.
    DOI:  https://doi.org/10.1097/HS9.0000000000000895
  30. Cell Death Dis. 2023 Jun 10. 14(6): 357
      Pediatric Acute Myeloid Leukemia (AML) is a rare and heterogeneous disease characterized by a high prevalence of gene fusions as driver mutations. Despite the improvement of survival in the last years, about 50% of patients still experience a relapse. It is not possible to improve prognosis only with further intensification of chemotherapy, as come with a severe cost to the health of patients, often resulting in treatment-related death or long-term sequels. To design more effective and less toxic therapies we need a better understanding of pediatric AML biology. The NUP98-KDM5A chimeric protein is exclusively found in a particular subgroup of young pediatric AML patients with complex karyotypes and poor prognosis. In this study, we investigated the impact of NUP98-KDM5A expression on cellular processes in human Pluripotent Stem Cell models and a patient-derived cell line. We found that NUP98-KDM5A generates genomic instability through two complementary mechanisms that involve accumulation of DNA damage and direct interference of RAE1 activity during mitosis. Overall, our data support that NUP98-KDM5A promotes genomic instability and likely contributes to malignant transformation.
    DOI:  https://doi.org/10.1038/s41419-023-05870-5
  31. Hemasphere. 2023 Jun;7(6): e912
      Altering the natural history of acute myeloid leukemia (AML) in unfit and older patients has proved a highly challenging hurdle, despite several decades of concerted clinical trial effort. The arrival of venetoclax (VEN) to the clinical stage represents the most important therapeutic advance to date for older patients with AML. In this review, we will explain how and why VEN works, summarize its remarkable pathway to regulatory approval, and highlight the key milestones that have been important for its successful development in AML. We also provide perspectives on some of the challenges associated with using VEN in the clinic, emerging knowledge regarding mechanisms of treatment failure, and current clinical research directions likely to shape how this drug and others in this new class of anticancer agents are used in the future.
    DOI:  https://doi.org/10.1097/HS9.0000000000000912
  32. Cancer Cell. 2023 May 16. pii: S1535-6108(23)00169-1. [Epub ahead of print]
      The first step of oncogenesis is the acquisition of a repertoire of genetic mutations to initiate and sustain the malignancy. An important example of this initiation phase in acute leukemias is the formation of a potent oncogene by chromosomal translocations between the mixed lineage leukemia (MLL) gene and one of 100 translocation partners, known as the MLL recombinome. Here, we show that circular RNAs (circRNAs)-a family of covalently closed, alternatively spliced RNA molecules-are enriched within the MLL recombinome and can bind DNA, forming circRNA:DNA hybrids (circR loops) at their cognate loci. These circR loops promote transcriptional pausing, proteasome inhibition, chromatin re-organization, and DNA breakage. Importantly, overexpressing circRNAs in mouse leukemia xenograft models results in co-localization of genomic loci, de novo generation of clinically relevant chromosomal translocations mimicking the MLL recombinome, and hastening of disease onset. Our findings provide fundamental insight into the acquisition of chromosomal translocations by endogenous RNA carcinogens in leukemia.
    Keywords:  MLL fusions; R-loops; RNA interactome; RNA splicing; acute myeloid leukemia; chromosomal translocations; circular RNAs; genome instability; leukemia; proteasome
    DOI:  https://doi.org/10.1016/j.ccell.2023.05.002
  33. Cancers (Basel). 2023 May 27. pii: 2942. [Epub ahead of print]15(11):
      Optical genome mapping (OGM) recently has demonstrated the potential to improve genetic diagnostics in acute myeloid leukemia (AML). In this study, OGM was utilized as a tool for the detection of genome-wide structural variants and disease monitoring. A previously unrecognized NUP98::ASH1L fusion was detected in an adult patient with secondary AML. OGM identified the fusion of NUP98 to Absent, Small, or Homeotic-Like Histone Lysine Methyltransferase (ASH1L) as result of a complex structural rearrangement between chromosomes 1 and 11. A pipeline for the measurement of rare structural variants (Rare Variant Pipeline, Bionano Genomics, San Diego, CA, USA) was used for detection. As NUP98 and other fusions are relevant for disease classification, this demonstrates the necessity for methods such as OGM for cytogenetic diagnostics in AML. Furthermore, other structural variants showed discordant variant allele frequencies at different time points over the course of the disease and treatment pressure, indicating clonal evolution. These results support OGM to be a valuable tool for primary diagnostics in AML as well as longitudinal testing for disease monitoring and deepening our understanding of genetically heterogenous diseases.
    Keywords:  clonal evolution; cytogenetics; disease monitoring: structural variants; karyotyping; rare variant pipeline
    DOI:  https://doi.org/10.3390/cancers15112942
  34. J Clin Invest. 2023 06 15. pii: e171104. [Epub ahead of print]133(12):
      Palmitoylation is a critical posttranslational modification that enables the cellular membrane localization and subsequent activation of RAS proteins, including HRAS, KRAS, and NRAS. However, the molecular mechanism that regulates RAS palmitoylation in malignant diseases remains unclear. In this issue of the JCI, Ren, Xing, and authors shed light on this topic and revealed how upregulation of RAB27B, as a consequence of CBL loss and Janus kinase 2 (JAK2) activation, contributes to leukemogenesis. The authors found that RAB27B mediated NRAS palmitoylation and plasma membrane localization by recruiting ZDHHC9. The findings suggest that targeting RAB27B could provide a promising therapeutic strategy for NRAS-driven cancers.
    DOI:  https://doi.org/10.1172/JCI171104
  35. Am J Hematol. 2023 Jul;98(7): 1097-1116
       OVERVIEW: Systemic mastocytosis (SM) results from clonal proliferation of mast cells (MC) in extracutaneous organs.
    DIAGNOSIS: The major criterion is presence of multifocal MC clusters in the bone marrow and/or extracutaneous organs. Minor diagnostic criteria include elevated serum tryptase level, MC CD25/CD2/CD30 expression, and presence of activating KIT mutations.
    RISK STRATIFICATION: Establishing SM subtype as per the International Consensus Classification/World Health Organization classification systems is an important first step. Patients either have indolent/smoldering SM (ISM/SSM) or advanced SM, including aggressive SM (ASM), SM with associated myeloid neoplasm (SM-AMN), and mast cell leukemia. Identification of poor-risk mutations (i.e., ASXL1, RUNX1, SRSF2, NRAS) further refines the risk stratification. Several risk models are available to help assign prognosis in SM patients.
    MANAGEMENT: Treatment goals for ISM patients are primarily directed toward anaphylaxis prevention/symptom control/osteoporosis treatment. Patients with advanced SM frequently need MC cytoreductive therapy to reverse disease-related organ dysfunction. Tyrosine kinase inhibitors (TKI) (midostaurin, avapritinib) have changed the treatment landscape in SM. While deep biochemical, histological and molecular responses have been documented with avapritinib treatment, its efficacy as monotherapy against a multimutated AMN disease component in SM-AMN patients remains unclear. Cladribine continues to have a role for MC debulking, whereas interferon-α has a diminishing role in the TKI era. Treatment of SM-AMN primarily targets the AMN component, particularly if an aggressive disease such as acute leukemia is present. Allogeneic stem cell transplant has a role in such patients. Imatinib has a therapeutic role only in the rare patient with an imatinib-sensitive KIT mutation.
    DOI:  https://doi.org/10.1002/ajh.26962
  36. Blood. 2023 Jun 15. pii: blood.2023020035. [Epub ahead of print]
      In the "ABA2" study, the T-cell costimulation blockade agent, abatacept, was safe and effective in preventing acute graft-versus-host disease (AGVHD) after unrelated-donor hematopoietic cell transplantation (URD HCT), leading to FDA approval. Here, we performed a detailed determination of abatacept pharmacokinetics (PK), which enabled an examination of how abatacept exposure-response (E-R) relationships impacted key clinical outcomes. To accomplish this, we performed a population PK analysis of intravenous abatacept using nonlinear mixed-effect modeling, and assessed the association between abatacept exposure (dosed at 10 mg/kg on Days -1,+5,+14,+28) and key transplant outcomes. We tested the association between the trough concentration after dose 1 (Ctrough_1) and Grade 2-4 acute GVHD (Gr 2-4 AGVHD) through Day+100 as the primary outcome in 184 HCT patients. An optimal Ctrough_1 threshold was identified by recursive partitioning and classification tree analysis. This demonstrated that abatacept PK was characterized by a two-compartment model with first-order elimination. The ABA2 dosing regimen was based on previous work targeting a steady-state abatacept trough of 10 μg/mL. However, a higher Ctrough_1 (≥39μg/mL, attained in ~60% of ABA2 patients) was associated with a favorable Gr 2-4 AGVHD risk (HR:0.35, 95%CI:0.19-0.65, p<0.001), with a Ctrough_1 <39μg/mL associated with Gr 2-4 AGVHD risk indistinguishable from placebo (p=0.37). Importantly, no significant association was found between Ctrough_1 and key safety indicators, including relapse, CMV viremia, and EBV viremia. These data demonstrate that, compared to a previously reported target Ctrough_1 of 10 μg/mL, a higher abatacept Ctrough_1 (≥39 μg/mL) was associated with a favorable Gr 2-4 AGVHD risk, without any observed exposure-toxicity relationships. Clinical trial NCT01743131.
    DOI:  https://doi.org/10.1182/blood.2023020035