The mTOR inhibitor everolimus overcomes CXCR4-mediated resistance to histone deacetylase inhibitor panobinostat through inhibition of p21 and mitotic regulators.


Journal

Biochemical pharmacology
ISSN: 1873-2968
Titre abrégé: Biochem Pharmacol
Pays: England
ID NLM: 0101032

Informations de publication

Date de publication:
10 2019
Historique:
received: 14 05 2019
accepted: 15 07 2019
pubmed: 22 7 2019
medline: 2 7 2020
entrez: 21 7 2019
Statut: ppublish

Résumé

Although having promising anti-myeloma properties, the pan-histone deacetylase inhibitor (HDACi) panobinostat lacks therapeutic activity as a single agent. The aim of the current study was to elucidate the mechanisms underlying multiple myeloma (MM) resistance to panobinostat monotherapy and to define strategies to overcome it. Sensitivity of MM cell lines and primary CD138+ cells from MM patients to panobinostat correlated with reduced expression of the chemokine receptor CXCR4, whereas overexpression of CXCR4 in MM cell lines increased their resistance to panobinostat. Decreased sensitivity to HDACi was associated with reversible G0/G1 cell growth arrest while response was characterized by apoptotic cell death. Analysis of intra-cellular signaling mediators revealed the pro-survival mTOR pathway to be regulated by CXCR4 overexpression. Combining panobinostat with mTOR inhibitor everolimus abrogated the resistance to HDACi and induced synergistic cell death. The combination of panobinostat/everolimus resulted in sustained DNA damage and irreversible suppression of proliferation accompanied by robust apoptosis. Gene expression analysis revealed distinct genetic profiles of single versus combined agent exposure. Whereas panobinostat increased the expression of the cell cycle inhibitor p21, co-treatment with everolimus abrogated the increase in p21 and synergistically downregulated the expression of DNA repair genes and mitotic checkpoint regulators. Importantly, the combination of panobinostat with everolimus effectively targeted CXCR4-expressing resistant MM cells in vivo in the BM niche. In summary, our results uncover the mechanism responsible for the strong synergistic anti-MM activity of dual HDAC and mTOR inhibition and provide the rationale for a novel potential therapeutic approach to treat MM.

Identifiants

pubmed: 31325448
pii: S0006-2952(19)30271-0
doi: 10.1016/j.bcp.2019.07.016
pii:
doi:

Substances chimiques

Antineoplastic Agents 0
CXCR4 protein, human 0
Histone Deacetylase Inhibitors 0
Receptors, CXCR4 0
Panobinostat 9647FM7Y3Z
Everolimus 9HW64Q8G6G
MTOR protein, human EC 2.7.1.1
TOR Serine-Threonine Kinases EC 2.7.11.1
rho GTP-Binding Proteins EC 3.6.5.2

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

412-428

Informations de copyright

Copyright © 2019 Elsevier Inc. All rights reserved.

Auteurs

Katia Beider (K)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Ramat Gan, Tel Aviv University, Israel.

Hanna Bitner (H)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Ramat Gan, Tel Aviv University, Israel.

Valeria Voevoda-Dimenshtein (V)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Ramat Gan, Tel Aviv University, Israel.

Evgenia Rosenberg (E)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Ramat Gan, Tel Aviv University, Israel.

Yaarit Sirovsky (Y)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Ramat Gan, Tel Aviv University, Israel.

Hila Magen (H)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Ramat Gan, Tel Aviv University, Israel.

Jonathan Canaani (J)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Ramat Gan, Tel Aviv University, Israel.

Olga Ostrovsky (O)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Ramat Gan, Tel Aviv University, Israel.

Noya Shilo (N)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Ramat Gan, Tel Aviv University, Israel.

Avichai Shimoni (A)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Ramat Gan, Tel Aviv University, Israel.

Michal Abraham (M)

Goldyne Savad Institute of Gene Therapy, Hebrew University Hospital, Jerusalem, Israel.

Lola Weiss (L)

Goldyne Savad Institute of Gene Therapy, Hebrew University Hospital, Jerusalem, Israel.

Michael Milyavsky (M)

Department of Pathology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.

Amnon Peled (A)

Goldyne Savad Institute of Gene Therapy, Hebrew University Hospital, Jerusalem, Israel.

Arnon Nagler (A)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Ramat Gan, Tel Aviv University, Israel. Electronic address: Arnon.Nagler@sheba.health.gov.il.

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Classifications MeSH