Activation of RAS/MAPK pathway confers MCL-1 mediated acquired resistance to BCL-2 inhibitor venetoclax in acute myeloid leukemia.


Journal

Signal transduction and targeted therapy
ISSN: 2059-3635
Titre abrégé: Signal Transduct Target Ther
Pays: England
ID NLM: 101676423

Informations de publication

Date de publication:
21 02 2022
Historique:
received: 13 10 2020
accepted: 20 12 2021
revised: 01 11 2021
entrez: 21 2 2022
pubmed: 22 2 2022
medline: 5 4 2022
Statut: epublish

Résumé

Despite high initial response rates, acute myeloid leukemia (AML) treated with the BCL-2-selective inhibitor venetoclax (VEN) alone or in combinations commonly acquires resistance. We performed gene/protein expression, metabolomic and methylation analyses of isogenic AML cell lines sensitive or resistant to VEN, and identified the activation of RAS/MAPK pathway, leading to increased stability and higher levels of MCL-1 protein, as a major acquired mechanism of VEN resistance. MCL-1 sustained survival and maintained mitochondrial respiration in VEN-RE cells, which had impaired electron transport chain (ETC) complex II activity, and MCL-1 silencing or pharmacologic inhibition restored VEN sensitivity. In support of the importance of RAS/MAPK activation, we found by single-cell DNA sequencing rapid clonal selection of RAS-mutated clones in AML patients treated with VEN-containing regimens. In summary, these findings establish RAS/MAPK/MCL-1 and mitochondrial fitness as key survival mechanisms of VEN-RE AML and provide the rationale for combinatorial strategies effectively targeting these pathways.

Identifiants

pubmed: 35185150
doi: 10.1038/s41392-021-00870-3
pii: 10.1038/s41392-021-00870-3
pmc: PMC8858957
doi:

Substances chimiques

BCL2 protein, human 0
Bridged Bicyclo Compounds, Heterocyclic 0
MCL1 protein, human 0
Myeloid Cell Leukemia Sequence 1 Protein 0
Proto-Oncogene Proteins c-bcl-2 0
Sulfonamides 0
ras Proteins EC 3.6.5.2
venetoclax N54AIC43PW

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

51

Subventions

Organisme : NCI NIH HHS
ID : R35 CA242427
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA016672
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA235622
Pays : United States
Organisme : NCI NIH HHS
ID : P50 CA100632
Pays : United States
Organisme : NCI NIH HHS
ID : U54 CA224019
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA066996
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA262758
Pays : United States

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2022. The Author(s).

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Auteurs

Qi Zhang (Q)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Bridget Riley-Gillis (B)

AbbVie Inc., North Chicago, IL, USA.

Lina Han (L)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Yannan Jia (Y)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
Institute of Hematology, Chinese Academy of Medical Sciences & Peking Union Medical College, Tianjin, China.

Alessia Lodi (A)

Department of Nutritional Sciences, Department of Pediatrics, Department of Oncology, Dell Medical School, The University of Texas at Austin, Austin, TX, 78712, USA.

Haijiao Zhang (H)

Department of Cell, Developmental & Cancer Biology, Division of Hematology & Medical Oncology, Knight Cancer Institute, Oregon Health & Science University, Portland, OR, USA.

Saravanan Ganesan (S)

Université de Paris, Institut de la Recherche Saint-Louis (IRSL), Inserm Unit 1131, Paris, France.

Rongqing Pan (R)

Dana-Farber Cancer Institute, Boston, MA, USA.

Sergej N Konoplev (SN)

Department of Hematopathology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Shannon R Sweeney (SR)

Department of Nutritional Sciences, Department of Pediatrics, Department of Oncology, Dell Medical School, The University of Texas at Austin, Austin, TX, 78712, USA.

Jeremy A Ryan (JA)

Dana-Farber Cancer Institute, Boston, MA, USA.

Yulia Jitkova (Y)

Princess Margaret Cancer Center, Toronto, ON, Canada.

Kenneth Dunner (K)

High Resolution Electron Microscopy Facility, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Shaun E Grosskurth (SE)

AbbVie Inc., North Chicago, IL, USA.

Priyanka Vijay (P)

AbbVie Inc., North Chicago, IL, USA.

Sujana Ghosh (S)

AbbVie Inc., North Chicago, IL, USA.

Charles Lu (C)

AbbVie Inc., North Chicago, IL, USA.

Wencai Ma (W)

Department of Bioinformatics & Computational Biology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Stephen Kurtz (S)

Department of Cell, Developmental & Cancer Biology, Division of Hematology & Medical Oncology, Knight Cancer Institute, Oregon Health & Science University, Portland, OR, USA.

Vivian R Ruvolo (VR)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Helen Ma (H)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Connie C Weng (CC)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Cassandra L Ramage (CL)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Natalia Baran (N)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Ce Shi (C)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
Department of Hematology, The First Hospital Affiliated Harbin Medical University, Harbin, China.

Tianyu Cai (T)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Richard Eric Davis (RE)

Department of Lymphoma & Myeloma Research, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Venkata L Battula (VL)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Yingchang Mi (Y)

Institute of Hematology, Chinese Academy of Medical Sciences & Peking Union Medical College, Tianjin, China.

Jing Wang (J)

Department of Bioinformatics & Computational Biology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Courtney D DiNardo (CD)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Michael Andreeff (M)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Jeffery W Tyner (JW)

Department of Cell, Developmental & Cancer Biology, Division of Hematology & Medical Oncology, Knight Cancer Institute, Oregon Health & Science University, Portland, OR, USA.

Aaron Schimmer (A)

Department of Hematopathology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Anthony Letai (A)

Dana-Farber Cancer Institute, Boston, MA, USA.

Rose Ann Padua (RA)

Université de Paris, Institut de la Recherche Saint-Louis (IRSL), Inserm Unit 1131, Paris, France.

Carlos E Bueso-Ramos (CE)

Department of Hematopathology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Stefano Tiziani (S)

Department of Nutritional Sciences, Department of Pediatrics, Department of Oncology, Dell Medical School, The University of Texas at Austin, Austin, TX, 78712, USA.

Joel Leverson (J)

AbbVie Inc., North Chicago, IL, USA.

Relja Popovic (R)

AbbVie Inc., North Chicago, IL, USA.

Marina Konopleva (M)

Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA. mkonople@mdanderson.org.

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