PAX5 fusion genes are frequent in poor risk childhood acute lymphoblastic leukaemia and can be targeted with BIBF1120.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Sep 2022
Historique:
received: 28 02 2022
revised: 07 07 2022
accepted: 30 07 2022
pubmed: 20 8 2022
medline: 21 9 2022
entrez: 19 8 2022
Statut: ppublish

Résumé

Despite intensive risk-based treatment protocols, 15% of paediatric patients with B-Cell Precursor Acute Lymphoblastic Leukaemia (BCP-ALL) experience relapse. There is urgent need of novel strategies to target poor prognosis subgroups, like PAX5 translocated. We considered 289 childhood BCP-ALL cases consecutively enrolled in Italy in the AIEOP-BFM ALL2000/R2006 protocols and we performed extensive molecular profiling, integrating gene expression, copy number analyses and fusion genes discovery by target-capture NGS. We developed preclinical strategies to target PAX5 fusion genes. We identified 135 cases without recurrent genetic rearrangements. Among them, 59 patients (43·7%) had a Ph-like signature; the remaining cases were identified as ERG-related (26%), High-Hyperdiploid-like (17%), ETV6::RUNX1-like (8·9%), MEF2D-rearranged (2·2%) or KMT2A-like (1·5%). A poor prognosis was associated with the Ph-like signature, independently from other high-risk features. Interestingly, PAX5 was altered in 54·4% of Ph-like compared to 16·2% of non-Ph-like cases, with 7 patients carrying PAX5 fusions (PAX5t), involving either novel (ALDH18A1, IKZF1, CDH13) or known (FBRSL1, AUTS2, DACH2) partner genes. PAX5t cases have a specific driver activity signature, extending to multiple pathways including LCK hyperactivation. Among FDA-approved drugs and inhibitors, we selected Dasatinib, Bosutinib and Foretinib, in addition to Nintedanib, known to be LCK ligands. We demonstrated the efficacy of the LCK-inhibitor BIBF1120/Nintedanib, as single agent or in combination with conventional chemotherapy, both ex vivo and in patient-derived xenograft model, showing a synergistic effect with dexamethasone. This study provides new insights in high-risk Ph-like leukaemia and identifies a potential therapy for targeting PAX5-fusion poor risk group. Ricerca Finalizzata-Giovani Ricercatori (Italian Ministry of Health), AIRC, Transcall, Fondazione Cariparo.

Sections du résumé

BACKGROUND BACKGROUND
Despite intensive risk-based treatment protocols, 15% of paediatric patients with B-Cell Precursor Acute Lymphoblastic Leukaemia (BCP-ALL) experience relapse. There is urgent need of novel strategies to target poor prognosis subgroups, like PAX5 translocated.
METHODS METHODS
We considered 289 childhood BCP-ALL cases consecutively enrolled in Italy in the AIEOP-BFM ALL2000/R2006 protocols and we performed extensive molecular profiling, integrating gene expression, copy number analyses and fusion genes discovery by target-capture NGS. We developed preclinical strategies to target PAX5 fusion genes.
FINDINGS RESULTS
We identified 135 cases without recurrent genetic rearrangements. Among them, 59 patients (43·7%) had a Ph-like signature; the remaining cases were identified as ERG-related (26%), High-Hyperdiploid-like (17%), ETV6::RUNX1-like (8·9%), MEF2D-rearranged (2·2%) or KMT2A-like (1·5%). A poor prognosis was associated with the Ph-like signature, independently from other high-risk features. Interestingly, PAX5 was altered in 54·4% of Ph-like compared to 16·2% of non-Ph-like cases, with 7 patients carrying PAX5 fusions (PAX5t), involving either novel (ALDH18A1, IKZF1, CDH13) or known (FBRSL1, AUTS2, DACH2) partner genes. PAX5t cases have a specific driver activity signature, extending to multiple pathways including LCK hyperactivation. Among FDA-approved drugs and inhibitors, we selected Dasatinib, Bosutinib and Foretinib, in addition to Nintedanib, known to be LCK ligands. We demonstrated the efficacy of the LCK-inhibitor BIBF1120/Nintedanib, as single agent or in combination with conventional chemotherapy, both ex vivo and in patient-derived xenograft model, showing a synergistic effect with dexamethasone.
INTERPRETATION CONCLUSIONS
This study provides new insights in high-risk Ph-like leukaemia and identifies a potential therapy for targeting PAX5-fusion poor risk group.
FUNDING BACKGROUND
Ricerca Finalizzata-Giovani Ricercatori (Italian Ministry of Health), AIRC, Transcall, Fondazione Cariparo.

Identifiants

pubmed: 35985167
pii: S2352-3964(22)00406-6
doi: 10.1016/j.ebiom.2022.104224
pmc: PMC9403348
pii:
doi:

Substances chimiques

Core Binding Factor Alpha 2 Subunit 0
Indoles 0
PAX5 Transcription Factor 0
PAX5 protein, human 0
Dexamethasone 7S5I7G3JQL
nintedanib G6HRD2P839
Dasatinib RBZ1571X5H

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104224

Subventions

Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing financial interests.

Auteurs

Grazia Fazio (G)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy. Electronic address: grazia.fazio@unimib.it.

Silvia Bresolin (S)

Paediatric Haematology, Oncology and Stem Cell Transplant Division, Women and Child Health Department, Padua University and Hospital, Padua, Italy.

Daniela Silvestri (D)

Centre of Biostatistics for Clinical Epidemiology, School of Medicine and Surgery, University of Milano-Bicocca, Monza, Italy.

Manuel Quadri (M)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy.

Claudia Saitta (C)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy.

Elena Vendramini (E)

Paediatric Haematology, Oncology and Stem Cell Transplant Division, Women and Child Health Department, Padua University and Hospital, Padua, Italy.

Barbara Buldini (B)

Paediatric Haematology, Oncology and Stem Cell Transplant Division, Women and Child Health Department, Padua University and Hospital, Padua, Italy.

Chiara Palmi (C)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy.

Michela Bardini (M)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy.

Andrea Grioni (A)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy.

Silvia Rigamonti (S)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy.

Marta Galbiati (M)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy.

Stefano Mecca (S)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy.

Angela Maria Savino (AM)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy; Molecular Pharmacology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.

Alberto Peloso (A)

Paediatric Haematology, Oncology and Stem Cell Transplant Division, Women and Child Health Department, Padua University and Hospital, Padua, Italy.

Jia-Wey Tu (JW)

Department of Paediatric Oncology, Haematology and Clinical Immunology, Heinrich-Heine University Dusseldorf, Medical Faculty, Düsseldorf, Germany.

Sanil Bhatia (S)

Department of Paediatric Oncology, Haematology and Clinical Immunology, Heinrich-Heine University Dusseldorf, Medical Faculty, Düsseldorf, Germany.

Arndt Borkhardt (A)

Department of Paediatric Oncology, Haematology and Clinical Immunology, Heinrich-Heine University Dusseldorf, Medical Faculty, Düsseldorf, Germany.

Concetta Micalizzi (C)

Haematology/Oncology Unit, G. Gaslini Children's Hospital, Genoa, Italy.

Luca Lo Nigro (L)

Center of Paediatric Haematology Oncology, Azienda Ospedaliero-Universitaria "Policlinico Vittorio Emanuele", Catania, Italy.

Franco Locatelli (F)

Department of Paediatric Haematology/Oncology and Cell and Gene Therapy, IRCCS Ospedale Pediatrico Bambino Gesù, Department of Paediatrics, Sapienza University of Rome, Rome, Italy.

Valentino Conter (V)

Paediatrics, University of Milano Bicocca, Fondazione MBBM/San Gerardo Hospital, Monza, Italy.

Carmelo Rizzari (C)

Paediatrics, University of Milano Bicocca, Fondazione MBBM/San Gerardo Hospital, Monza, Italy.

Maria Grazia Valsecchi (MG)

Centre of Biostatistics for Clinical Epidemiology, School of Medicine and Surgery, University of Milano-Bicocca, Monza, Italy.

Geertruij Te Kronnie (G)

Paediatric Haematology, Oncology and Stem Cell Transplant Division, Women and Child Health Department, Padua University and Hospital, Padua, Italy.

Andrea Biondi (A)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy; Paediatrics, University of Milano Bicocca, Fondazione MBBM/San Gerardo Hospital, Monza, Italy.

Giovanni Cazzaniga (G)

Centro Ricerca M. Tettamanti, Paediatrics, University of Milano Bicocca, Monza, Italy; Medical Genetics, University of Milano Bicocca, School of Medicine and Surgery, Monza, Italy. Electronic address: giovanni.cazzaniga@unimib.it.

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