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Dissecting the role of TP53 alterations in del(11q) chronic lymphocytic leukemia

Dissecting the role of TP53 alterations in del(11q) chronic lymphocytic leukemia
Dissecting the role of TP53 alterations in del(11q) chronic lymphocytic leukemia
Background: Several genetic alterations have been identified as driver events
in chronic lymphocytic leukemia (CLL) pathogenesis and oncogenic evolution.
Concurrent driver alterations usually coexist within the same tumoral clone,
but how the cooperation of multiple genomic abnormalities contributes to disease
progression remains poorly understood. Specifically, the biological and clinical
consequences of concurrent high-risk alterations such as del(11q)/ATMmutations
and del(17p)/TP53-mutations have not been established.
Methods:We integrated next-generation sequencing (NGS) and clustered regularly
interspaced short palindromic repeats (CRISPR)/Cas9 techniques to characterize
the in vitro and in vivo effects of concurrent monoallelic or biallelic
ATM and/or TP53 alterations in CLL prognosis, clonal evolution, and therapy
response.
Results: Targeted sequencing analysis of the co-occurrence of high-risk alterations
in 271 CLLs revealed that biallelic inactivation of both ATM and TP53 was
mutually exclusive, whereas monoallelic del(11q) and TP53 alterations significantly
co-occurred in a subset of CLL patients with a highly adverse clinical outcome.
We determined the biological effects of combined del(11q), ATM and/or
TP53 mutations in CRISPR/Cas9-edited CLL cell lines. Our results showed that
the combination of monoallelic del(11q) and TP53 mutations in CLL cells led
to a clonal advantage in vitro and in in vivo clonal competition experiments,
whereas CLL cells harboring biallelic ATM and TP53 loss failed to compete in
in vivo xenotransplants. Furthermore, we demonstrated that CLL cell lines harboring
del(11q) and TP53 mutations show only partial responses to B cell receptor
signaling inhibitors, but may potentially benefit from ATR inhibition.
Conclusions: Ourwork highlights that combinedmonoallelic del(11q) and TP53
alterations coordinately contribute to clonal advantage and shorter overall survival
in CLL.
Adult, Aged, Aged, 80 and over, Animals, Chromosome Deletion, Disease Models, Animal, Disease Progression, Female, High-Throughput Nucleotide Sequencing/methods, Humans, Leukemia, Lymphocytic, Chronic, B-Cell/genetics, Male, Mice, Middle Aged, Mutation/genetics, Prognosis, Tumor Suppressor Protein p53/genetics
e304
Quijada‐álamo, Miguel
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Pérez‐carretero, Claudia
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Hernández‐sánchez, María
48fccfbf-6e3d-46e9-830c-1a2fcedef69a
Rodríguez‐vicente, Ana‐eugenia
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Herrero, Ana‐belén
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Hernández‐sánchez, Jesús‐maría
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Martín‐izquierdo, Marta
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Santos‐mínguez, Sandra
cdf622f9-078e-4ab3-ae57-0e093ac1cc13
Del Rey, Mónica
d83eb31c-cde7-4236-b84f-771e3bd4d67e
González, Teresa
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Rubio‐martínez, Araceli
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García De Coca, Alfonso
fc3bf992-6270-47e8-9e27-e3ce9bc9c09e
Dávila‐valls, Julio
35347601-74f0-417f-8f80-96b892149cee
Hernández‐rivas, José‐ángel
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Parker, Helen
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Strefford, Jonathan C.
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Benito, Rocío
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Ordóñez, José‐luis
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Hernández‐rivas, Jesús‐maría
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Quijada‐álamo, Miguel
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Pérez‐carretero, Claudia
8a9fb35a-0159-481f-8783-dfc3333d227d
Hernández‐sánchez, María
48fccfbf-6e3d-46e9-830c-1a2fcedef69a
Rodríguez‐vicente, Ana‐eugenia
730ad1af-5dc4-4592-8818-718572af97f9
Herrero, Ana‐belén
9d0c5c99-7995-4371-b356-ca5d726cc239
Hernández‐sánchez, Jesús‐maría
b720b145-815b-4431-8a2d-2acb55e370b9
Martín‐izquierdo, Marta
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Santos‐mínguez, Sandra
cdf622f9-078e-4ab3-ae57-0e093ac1cc13
Del Rey, Mónica
d83eb31c-cde7-4236-b84f-771e3bd4d67e
González, Teresa
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Rubio‐martínez, Araceli
02d4371e-7b02-40ed-bce5-6195ce8239c0
García De Coca, Alfonso
fc3bf992-6270-47e8-9e27-e3ce9bc9c09e
Dávila‐valls, Julio
35347601-74f0-417f-8f80-96b892149cee
Hernández‐rivas, José‐ángel
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Parker, Helen
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Strefford, Jonathan C.
3782b392-f080-42bf-bdca-8aa5d6ca532f
Benito, Rocío
8c2b3e75-e1ee-43d1-84c2-93b8e0fc3ae8
Ordóñez, José‐luis
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Hernández‐rivas, Jesús‐maría
33b18033-d429-40dd-9d91-2a7bac51aa3c

Quijada‐álamo, Miguel, Pérez‐carretero, Claudia, Hernández‐sánchez, María, Rodríguez‐vicente, Ana‐eugenia, Herrero, Ana‐belén, Hernández‐sánchez, Jesús‐maría, Martín‐izquierdo, Marta, Santos‐mínguez, Sandra, Del Rey, Mónica, González, Teresa, Rubio‐martínez, Araceli, García De Coca, Alfonso, Dávila‐valls, Julio, Hernández‐rivas, José‐ángel, Parker, Helen, Strefford, Jonathan C., Benito, Rocío, Ordóñez, José‐luis and Hernández‐rivas, Jesús‐maría (2021) Dissecting the role of TP53 alterations in del(11q) chronic lymphocytic leukemia. Clinical and Translational Medicine, 11 (2), e304, [e304]. (doi:10.1002/ctm2.304).

Record type: Article

Abstract

Background: Several genetic alterations have been identified as driver events
in chronic lymphocytic leukemia (CLL) pathogenesis and oncogenic evolution.
Concurrent driver alterations usually coexist within the same tumoral clone,
but how the cooperation of multiple genomic abnormalities contributes to disease
progression remains poorly understood. Specifically, the biological and clinical
consequences of concurrent high-risk alterations such as del(11q)/ATMmutations
and del(17p)/TP53-mutations have not been established.
Methods:We integrated next-generation sequencing (NGS) and clustered regularly
interspaced short palindromic repeats (CRISPR)/Cas9 techniques to characterize
the in vitro and in vivo effects of concurrent monoallelic or biallelic
ATM and/or TP53 alterations in CLL prognosis, clonal evolution, and therapy
response.
Results: Targeted sequencing analysis of the co-occurrence of high-risk alterations
in 271 CLLs revealed that biallelic inactivation of both ATM and TP53 was
mutually exclusive, whereas monoallelic del(11q) and TP53 alterations significantly
co-occurred in a subset of CLL patients with a highly adverse clinical outcome.
We determined the biological effects of combined del(11q), ATM and/or
TP53 mutations in CRISPR/Cas9-edited CLL cell lines. Our results showed that
the combination of monoallelic del(11q) and TP53 mutations in CLL cells led
to a clonal advantage in vitro and in in vivo clonal competition experiments,
whereas CLL cells harboring biallelic ATM and TP53 loss failed to compete in
in vivo xenotransplants. Furthermore, we demonstrated that CLL cell lines harboring
del(11q) and TP53 mutations show only partial responses to B cell receptor
signaling inhibitors, but may potentially benefit from ATR inhibition.
Conclusions: Ourwork highlights that combinedmonoallelic del(11q) and TP53
alterations coordinately contribute to clonal advantage and shorter overall survival
in CLL.

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Accepted/In Press date: 18 January 2021
Published date: 4 February 2021
Additional Information: © 2021 The Authors. Clinical and Translational Medicine published by John Wiley & Sons Australia, Ltd on behalf of Shanghai Institute of Clinical Bioinformatics.
Keywords: Adult, Aged, Aged, 80 and over, Animals, Chromosome Deletion, Disease Models, Animal, Disease Progression, Female, High-Throughput Nucleotide Sequencing/methods, Humans, Leukemia, Lymphocytic, Chronic, B-Cell/genetics, Male, Mice, Middle Aged, Mutation/genetics, Prognosis, Tumor Suppressor Protein p53/genetics

Identifiers

Local EPrints ID: 447683
URI: http://eprints.soton.ac.uk/id/eprint/447683
PURE UUID: 3071f52c-1b74-4cda-a1dd-ffdebc7f6f3e
ORCID for Helen Parker: ORCID iD orcid.org/0000-0001-8308-9781
ORCID for Jonathan C. Strefford: ORCID iD orcid.org/0000-0002-0972-2881

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Date deposited: 18 Mar 2021 17:44
Last modified: 17 Mar 2024 02:59

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Contributors

Author: Miguel Quijada‐álamo
Author: Claudia Pérez‐carretero
Author: María Hernández‐sánchez
Author: Ana‐eugenia Rodríguez‐vicente
Author: Ana‐belén Herrero
Author: Jesús‐maría Hernández‐sánchez
Author: Marta Martín‐izquierdo
Author: Sandra Santos‐mínguez
Author: Mónica Del Rey
Author: Teresa González
Author: Araceli Rubio‐martínez
Author: Alfonso García De Coca
Author: Julio Dávila‐valls
Author: José‐ángel Hernández‐rivas
Author: Helen Parker ORCID iD
Author: Rocío Benito
Author: José‐luis Ordóñez
Author: Jesús‐maría Hernández‐rivas

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