Impact of BCR::ABL1 single nucleotide variants on asciminib efficacy.


Journal

Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895

Informations de publication

Date de publication:
17 Sep 2024
Historique:
received: 24 04 2024
accepted: 05 09 2024
revised: 28 08 2024
medline: 20 9 2024
pubmed: 20 9 2024
entrez: 19 9 2024
Statut: aheadofprint

Résumé

Asciminib is a potent and selective inhibitor of BCR::ABL1, with potential to avoid toxicity resulting from off-target kinase inhibition. Forty-nine patients treated with asciminib under a managed access program in the UK were evaluated for toxicity and response. Intolerance, rather than resistance (65% vs. 35%), was the most common reason for cessation of the last-line of treatment but asciminib was well tolerated, with most patients (29, 59%) remaining on treatment at a median of 14 months follow-up, and only 6 (12%) stopping for intolerance. Of 44 patients assessable for response, 29 (66%) achieved a complete cytogenetic response (CCyR) or better, with poorer responses seen in those stopping their last-line of therapy for resistance. Fewer patients with a prior history of a non-T315I-BCR::ABL1 single nucleotide variant (BSNV), or a non-T315I-BSNV detectable at baseline achieved CCyR. Serial tracking of BSNV by next generation sequencing demonstrated clonal expansion of BSNV-harbouring populations, which in some settings was associated with resistance (E459K, F317L, F359I), while in others was seen in the context of ongoing response, often with intensified dosing (T315I, I502F). These data suggest that asciminib exerts selective pressure on some BSNV-harbouring populations in vivo, some of which may respond to intensified dosing.

Identifiants

pubmed: 39300220
doi: 10.1038/s41375-024-02411-7
pii: 10.1038/s41375-024-02411-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Wylie AA, Schoepfer J, Jahnke W, Cowan-Jacob SW, Loo A, Furet P, et al. The allosteric inhibitor ABL001 enables dual targeting of BCR-ABL1. Nature 2017;543:733–7.
pubmed: 28329763 doi: 10.1038/nature21702
Bower H, Björkholm M, Dickman PW, Höglund M, Lambert PC, Andersson TM. Life expectancy of patients with chronic myeloid leukemia approaches the life expectancy of the general population. J Clin Oncol 2016;34:2851–7.
pubmed: 27325849 doi: 10.1200/JCO.2015.66.2866
Lipton JH, Brümmendorf TH, Gambacorti-Passerini C, Garcia-Gutiérrez V, Deininger MW, Cortes JE. Long-term safety review of tyrosine kinase inhibitors in chronic myeloid leukemia - What to look for when treatment-free remission is not an option. Blood Rev 2022;56:100968.
pubmed: 35570071 doi: 10.1016/j.blre.2022.100968
Pasvolsky O, Leader A, Iakobishvili Z, Wasserstrum Y, Kornowski R, Raanani P. Tyrosine kinase inhibitor associated vascular toxicity in chronic myeloid leukemia. Cardiooncology 2015;1:5.
pubmed: 33530148 pmcid: 7837152
Fabarius A, Giehl M, Rebacz B, Krämer A, Frank O, Haferlach C, et al. Centrosome aberrations and G1 phase arrest after in vitro and in vivo treatment with the SRC/ABL inhibitor dasatinib. Haematologica 2008;93:1145–54.
pubmed: 18519516 doi: 10.3324/haematol.12793
Shyam Sunder S, Sharma UC, Pokharel S. Adverse effects of tyrosine kinase inhibitors in cancer therapy: pathophysiology, mechanisms and clinical management. Signal Transduct Target Ther 2023;8:262.
pubmed: 37414756 pmcid: 10326056 doi: 10.1038/s41392-023-01469-6
Hantschel O, Nagar B, Guettler S, Kretzschmar J, Dorey K, Kuriyan J, et al. A myristoyl/phosphotyrosine switch regulates c-Abl. Cell 2003;112:845–57.
pubmed: 12654250 doi: 10.1016/S0092-8674(03)00191-0
Hughes TP, Mauro MJ, Cortes JE, Minami H, Rea D, DeAngelo DJ, et al. Asciminib in chronic myeloid leukemia after ABL kinase inhibitor failure. N. Engl J Med 2019;381:2315–26.
pubmed: 31826340 pmcid: 7724923 doi: 10.1056/NEJMoa1902328
Réa D, Mauro MJ, Boquimpani C, Minami Y, Lomaia E, Voloshin S, et al. A phase 3, open-label, randomized study of asciminib, a STAMP inhibitor, vs bosutinib in CML after 2 or more prior TKIs. Blood 2021;138:2031–41.
pubmed: 34407542 pmcid: 9728405 doi: 10.1182/blood.2020009984
Soverini S, Hochhaus A, Nicolini FE, Gruber F, Lange T, Saglio G, et al. BCR-ABL kinase domain mutation analysis in chronic myeloid leukemia patients treated with tyrosine kinase inhibitors: recommendations from an expert panel on behalf of European LeukemiaNet. Blood 2011;118:1208–15.
pubmed: 21562040 doi: 10.1182/blood-2010-12-326405
Schoepfer J, Jahnke W, Berellini G, Buonamici S, Cotesta S, Cowan-Jacob SW, et al. Discovery of Asciminib (ABL001), an allosteric inhibitor of the tyrosine kinase activity of BCR-ABL1. J Med Chem 2018;61:8120–35.
pubmed: 30137981 doi: 10.1021/acs.jmedchem.8b01040
Eide CA, Zabriskie MS, Savage Stevens SL, Antelope O, Vellore NA, Than H, et al. Combining the allosteric inhibitor asciminib with ponatinib suppresses emergence of and restores efficacy against highly resistant BCR-ABL1 mutants. Cancer Cell 2019;36:431–43.e5.
pubmed: 31543464 pmcid: 6893878 doi: 10.1016/j.ccell.2019.08.004
Mauro MJ, Hughes TP, Kim DW, Rea D, Cortes JE, Hochhaus A, et al. Asciminib monotherapy in patients with CML-CP without BCR::ABL1 T315I mutations treated with at least two prior TKIs: 4-year phase 1 safety and efficacy results. Leukemia 2023;37:1048–59.
pubmed: 36949155 pmcid: 10169635 doi: 10.1038/s41375-023-01860-w
Soverini S, Abruzzese E, Bocchia M, Bonifacio M, Galimberti S, Gozzini A, et al. Next-generation sequencing for BCR-ABL1 kinase domain mutation testing in patients with chronic myeloid leukemia: a position paper. J Hematol Oncol 2019;12:131.
pubmed: 31801582 pmcid: 6894351 doi: 10.1186/s13045-019-0815-5
Kizilors A, Crisà E, Lea N, Passera R, Mian S, Anwar J, et al. Effect of low-level BCR-ABL1 kinase domain mutations identified by next-generation sequencing in patients with chronic myeloid leukaemia: a population-based study. Lancet Haematol 2019;6:e276–84.
pubmed: 31036317 doi: 10.1016/S2352-3026(19)30027-4
Fernando F, Innes AJ, Claudiani S, Pryce A, Hayden C, Byrne J, et al. The outcome of post-transplant asciminib in patients with chronic myeloid leukaemia. Bone Marrow Transplant 2023;58:826–8.
pubmed: 37015970 doi: 10.1038/s41409-023-01975-9
Hochhaus A, Baccarani M, Silver RT, Schiffer C, Apperley JF, Cervantes F, et al. European LeukemiaNet 2020 recommendations for treating chronic myeloid leukemia. Leukemia 2020;34:966–84.
pubmed: 32127639 pmcid: 7214240 doi: 10.1038/s41375-020-0776-2
Cross NCP, Ernst T, Branford S, Cayuela JM, Deininger M, Fabarius A, et al. European LeukemiaNet laboratory recommendations for the diagnosis and management of chronic myeloid leukemia. Leukemia 2023;37:2150–67.
pubmed: 37794101 pmcid: 10624636 doi: 10.1038/s41375-023-02048-y
Hochhaus A, Réa D, Boquimpani C, Minami Y, Cortes JE, Hughes TP, et al. Asciminib vs bosutinib in chronic-phase chronic myeloid leukemia previously treated with at least two tyrosine kinase inhibitors: longer-term follow-up of ASCEMBL. Leukemia 2023;37:617–26.
pubmed: 36717654 pmcid: 9991909 doi: 10.1038/s41375-023-01829-9
Luna A, Pérez-Lamas L, Boque C, Giraldo P, Xicoy B, Ruiz Nuño C, et al. Real-life analysis on safety and efficacy of asciminib for ponatinib pretreated patients with chronic myeloid leukemia. Ann Hematol 2022;101:2263–70.
pubmed: 35997804 pmcid: 9463214 doi: 10.1007/s00277-022-04932-6
Kockerols CCB, Janssen J, Blijlevens NMA, Klein SK, Van Hussen-Daenen LGM, Van Gorkom GGY, et al. Treatment patterns and clinical outcomes of asciminib in a real-world multiresistant chronic myeloid leukemia patient population. Haematologica 2023;108:240–4.
pubmed: 36073515 doi: 10.3324/haematol.2022.281386
Khadadah FM, Cerquozzi S, Olney HJ, Fraga C, Dudebout J, Xenocostas A, et al. Canadian real-world experience of asciminib treatment in heavily pre-treated chronic myeloid leukemia (CML) patients who failed multiple lines of tyrosine kinase inhibitor (TKI) therapy. Leuk Res 2023;133:107374.
pubmed: 37657146 doi: 10.1016/j.leukres.2023.107374
Turkina AG, Shukhov OA, Lomaia E, Morozova EV, Petrova A, Chelysheva EY, et al. The First Results of Asciminib Therapy in Highly Pretreated Chronic Myeloid Leukemia Patients Under the Managed Access Program (MAP) in Russian Federation. Blood 2021;138:1483.
doi: 10.1182/blood-2021-145712
Qiang W, Antelope O, Zabriskie MS, Pomicter AD, Vellore NA, Szankasi P, et al. Mechanisms of resistance to the BCR-ABL1 allosteric inhibitor asciminib. Leukemia 2017;31:2844–7.
pubmed: 28819281 pmcid: 7566958 doi: 10.1038/leu.2017.264
Leyte-Vidal A, Garrido Ruiz D, DeFilippis R, Leske IB, Rea D, Phan S, et al. BCR::ABL1 Kinase N-lobe Mutants Confer Moderate to High Degrees of Resistance to Asciminib. Blood. 2024.

Auteurs

Andrew J Innes (AJ)

Centre for Haematology, Faculty of Medicine, Imperial College London, London, United Kingdom. a.innes@imperial.ac.uk.
Department of Haematology, Hammersmith Hospital, Imperial College Healthcare NHS Trust, London, United Kingdom. a.innes@imperial.ac.uk.

Chloe Hayden (C)

North West London Pathology, Hammersmith Hospital, Imperial College Healthcare NHS Trust, London, United Kingdom.

Victoria Orovboni (V)

North West London Pathology, Hammersmith Hospital, Imperial College Healthcare NHS Trust, London, United Kingdom.

Simone Claudiani (S)

Centre for Haematology, Faculty of Medicine, Imperial College London, London, United Kingdom.
Department of Haematology, Hammersmith Hospital, Imperial College Healthcare NHS Trust, London, United Kingdom.

Fiona Fernando (F)

Centre for Haematology, Faculty of Medicine, Imperial College London, London, United Kingdom.
Department of Haematology, Hammersmith Hospital, Imperial College Healthcare NHS Trust, London, United Kingdom.

Afzal Khan (A)

Centre for Haematology, Faculty of Medicine, Imperial College London, London, United Kingdom.
Department of Haematology, Hammersmith Hospital, Imperial College Healthcare NHS Trust, London, United Kingdom.

David Rees (D)

Medical School, Faculty of Medicine, Imperial College London, London, United Kingdom.

Jennifer Byrne (J)

Centre for Clinical Haematology, Nottingham University Hospitals NHS Trust, Nottingham, United Kingdom.

Paolo Gallipoli (P)

Centre for Haemato-Oncology, Barts Cancer Institute, Queen Mary University of London, London, United Kingdom.

Sebastian Francis (S)

Department of haematology, Sheffield Teaching Hospitals NHS Trust, Sheffield, United Kingdom.

Mhairi Copland (M)

Paul O'Gorman Leukaemia Research Centre, School of Cancer Sciences, University of Glasgow, Glasgow, United Kingdom.

Gillian Horne (G)

Paul O'Gorman Leukaemia Research Centre, School of Cancer Sciences, University of Glasgow, Glasgow, United Kingdom.

Manoj Raghavan (M)

Centre for Clinical Haematology, Queen Elizabeth Hospital, Birmingham, United Kingdom.

Claire Arnold (C)

Department of Haematology, Belfast City Hospital, Belfast, United Kingdom.

Angela Collins (A)

Department of Haematology, Norfolk and Norwich University Hospital, Norwich, United Kingdom.

Tanya Cranfield (T)

Department of Haematology, Queen Alexandra Hospital, Portsmouth, United Kingdom.

Nicholas Cunningham (N)

Department of Haematology, Belfast City Hospital, Belfast, United Kingdom.

Akila Danga (A)

Department of Haematology, The Hillingdon Hospital, London, United Kingdom.

Peter Forsyth (P)

Department of Haematology, Raigmore Hospital, NHS Highland, Inverness, United Kingdom.

Rebecca Frewin (R)

Department of Haematology, Gloucestershire Royal Hospital, Gloucester, United Kingdom.

Paula Garland (P)

Department of Haematology, Princess Royal University Hospital, London, United Kingdom.

Guy Hannah (G)

Department of Haematology, Kings College Hospital, London, United Kingdom.

Daniele Avenoso (D)

Department of Haematology, Kings College Hospital, London, United Kingdom.

Sandra Hassan (S)

Department of Haematology, Queen's Hospital, Romford, United Kingdom.

Brian J P Huntly (BJP)

Wellcome-MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge, United Kingdom.

Jissan Husain (J)

Department of Haematology, Ashford and St Peter's Hospitals NHS Foundation Trust, Chertsey, United Kingdom.

Sudhakaran Makkuni (S)

Department of Haematology, Mid and South Essex NHS Foundation Trust, Basildon, United Kingdom.

Kate Rothwell (K)

Department of Haematology, Leeds Teaching Hospitals NHS Trust, Basildon, United Kingdom.

Jamshid Khorashad (J)

Centre for Haematology, Faculty of Medicine, Imperial College London, London, United Kingdom.
Haemato-oncology Molecular Diagnostic Unit, The Royal Marsden Hospital NHS Foundation Trust, Sutton, United Kingdom.

Jane F Apperley (JF)

Centre for Haematology, Faculty of Medicine, Imperial College London, London, United Kingdom.
Department of Haematology, Hammersmith Hospital, Imperial College Healthcare NHS Trust, London, United Kingdom.

Dragana Milojkovic (D)

Centre for Haematology, Faculty of Medicine, Imperial College London, London, United Kingdom.
Department of Haematology, Hammersmith Hospital, Imperial College Healthcare NHS Trust, London, United Kingdom.

Classifications MeSH