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      Cotargeting of Mitochondrial Complex I and Bcl-2 Shows Antileukemic Activity against Acute Myeloid Leukemia Cells Reliant on Oxidative Phosphorylation

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          Abstract

          Targeting oxidative phosphorylation (OXPHOS) is a promising strategy to improve treatment outcomes of acute myeloid leukemia (AML) patients. IACS-010759 is a mitochondrial complex I inhibitor that has demonstrated preclinical antileukemic activity and is being tested in Phase I clinical trials. However, complex I deficiency has been reported to inhibit apoptotic cell death through prevention of cytochrome c release. Thus, combining IACS-010759 with a BH3 mimetic may overcome this mechanism of resistance leading to synergistic antileukemic activity against AML. In this study, we show that IACS-010759 and venetoclax synergistically induce apoptosis in OXPHOS-reliant AML cell lines and primary patient samples and cooperatively target leukemia progenitor cells. In a relatively OXPHOS-reliant AML cell line derived xenograft mouse model, IACS-010759 treatment significantly prolonged survival, which was further enhanced by treatment with IACS-010759 in combination with venetoclax. Consistent with our hypothesis, IACS-010759 treatment indeed retained cytochrome c in mitochondria, which was completely abolished by venetoclax, resulting in Bak/Bax- and caspase-dependent apoptosis. Our preclinical data provide a rationale for further development of the combination of IACS-010759 and venetoclax for the treatment of patients with AML.

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          An inhibitor of oxidative phosphorylation exploits cancer vulnerability

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            BCL-2 inhibition targets oxidative phosphorylation and selectively eradicates quiescent human leukemia stem cells.

            Most forms of chemotherapy employ mechanisms involving induction of oxidative stress, a strategy that can be effective due to the elevated oxidative state commonly observed in cancer cells. However, recent studies have shown that relative redox levels in primary tumors can be heterogeneous, suggesting that regimens dependent on differential oxidative state may not be uniformly effective. To investigate this issue in hematological malignancies, we evaluated mechanisms controlling oxidative state in primary specimens derived from acute myelogenous leukemia (AML) patients. Our studies demonstrate three striking findings. First, the majority of functionally defined leukemia stem cells (LSCs) are characterized by relatively low levels of reactive oxygen species (termed "ROS-low"). Second, ROS-low LSCs aberrantly overexpress BCL-2. Third, BCL-2 inhibition reduced oxidative phosphorylation and selectively eradicated quiescent LSCs. Based on these findings, we propose a model wherein the unique physiology of ROS-low LSCs provides an opportunity for selective targeting via disruption of BCL-2-dependent oxidative phosphorylation. Copyright © 2013 Elsevier Inc. All rights reserved.
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              Chemotherapy-Resistant Human Acute Myeloid Leukemia Cells Are Not Enriched for Leukemic Stem Cells but Require Oxidative Metabolism.

              Chemotherapy-resistant human acute myeloid leukemia (AML) cells are thought to be enriched in quiescent immature leukemic stem cells (LSC). To validate this hypothesis in vivo, we developed a clinically relevant chemotherapeutic approach treating patient-derived xenografts (PDX) with cytarabine (AraC). AraC residual AML cells are enriched in neither immature, quiescent cells nor LSCs. Strikingly, AraC-resistant preexisting and persisting cells displayed high levels of reactive oxygen species, showed increased mitochondrial mass, and retained active polarized mitochondria, consistent with a high oxidative phosphorylation (OXPHOS) status. AraC residual cells exhibited increased fatty-acid oxidation, upregulated CD36 expression, and a high OXPHOS gene signature predictive for treatment response in PDX and patients with AML. High OXPHOS but not low OXPHOS human AML cell lines were chemoresistant in vivo. Targeting mitochondrial protein synthesis, electron transfer, or fatty-acid oxidation induced an energetic shift toward low OXPHOS and markedly enhanced antileukemic effects of AraC. Together, this study demonstrates that essential mitochondrial functions contribute to AraC resistance in AML and are a robust hallmark of AraC sensitivity and a promising therapeutic avenue to treat AML residual disease.Significance: AraC-resistant AML cells exhibit metabolic features and gene signatures consistent with a high OXPHOS status. In these cells, targeting mitochondrial metabolism through the CD36-FAO-OXPHOS axis induces an energetic shift toward low OXPHOS and strongly enhanced antileukemic effects of AraC, offering a promising avenue to design new therapeutic strategies and fight AraC resistance in AML. Cancer Discov; 7(7); 716-35. ©2017 AACR.See related commentary by Schimmer, p. 670This article is highlighted in the In This Issue feature, p. 653.
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                Author and article information

                Journal
                Cancers (Basel)
                Cancers (Basel)
                cancers
                Cancers
                MDPI
                2072-6694
                24 August 2020
                September 2020
                : 12
                : 9
                : 2400
                Affiliations
                [1 ]National Engineering Laboratory for AIDS Vaccine, Key Laboratory for Molecular Enzymology and Engineering, School of Life Sciences, Jilin University, Changchun 130012, China; liufb18@ 123456mails.jlu.edu.cn (F.L.); majun17@ 123456mails.jlu.edu.cn (J.M.); suy@ 123456karmanos.org (Y.S.); lixy17@ 123456mails.jlu.edu.cn (X.L.)
                [2 ]Center for Molecular Medicine and Genetics, Wayne State University School of Medicine, Detroit, MI 48201, USA; hkalpage@ 123456med.wayne.edu (H.A.K.); mhuttema@ 123456med.wayne.edu (M.H.)
                [3 ]The Tumor Center of the First Hospital of Jilin University, Changchun 130021, China; DeYingW@ 123456hotmail.com
                [4 ]Department of Oncology, Wayne State University School of Medicine, Detroit, MI 48201, USA; pitmanh@ 123456karmanos.org (H.E.); polinl@ 123456karmanos.org (L.P.); kushnerj@ 123456karmanos.org (J.K.); dzinics@ 123456karmanos.org (S.H.D.); whitek@ 123456karmanos.org (K.W.)
                [5 ]Molecular Therapeutics Program, Barbara Ann Karmanos Cancer Institute, Wayne State University School of Medicine, Detroit, MI 48201, USA
                [6 ]Cancer Biology Graduate Program, Wayne State University School of Medicine, Detroit, MI 48201, USA; jenna.carter2@ 123456med.wayne.edu
                [7 ]Division of Pediatric Hematology/Oncology, Children’s Hospital of Michigan, Detroit, MI 48201, USA; jtaub@ 123456med.wayne.edu
                [8 ]Department of Pediatrics, Wayne State University School of Medicine, Detroit, MI 48201, USA
                Author notes
                [* ]Correspondence: wg10@ 123456jlu.edu.cn (G.W.); gey@ 123456karmanos.org (Y.G.)
                Author information
                https://orcid.org/0000-0002-5700-4884
                https://orcid.org/0000-0001-6310-7081
                https://orcid.org/0000-0003-1407-5778
                https://orcid.org/0000-0002-8748-716X
                Article
                cancers-12-02400
                10.3390/cancers12092400
                7564145
                32847115
                679a1d2d-c28f-40a2-860d-40d576dc1312
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 30 June 2020
                : 19 August 2020
                Categories
                Article

                acute myeloid leukemia,bcl-2,venetoclax,iacs-010759,oxidative phosphorylation

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