MLL-Rearranged Acute Lymphoblastic Leukemias Activate BCL-2 through H3K79 Methylation and Are Sensitive to the BCL-2-Specific Antagonist ABT-199
Targeted therapies designed to exploit specific molecular pathways in aggressive cancers are an exciting area of current research. Mixed Lineage Leukemia (MLL) mutations such as the t(4;11) translocation cause aggressive leukemias that are refractory to conventional treatment. The t(4;11) translocat...
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| Published in | Cell reports (Cambridge) Vol. 13; no. 12; pp. 2715 - 2727 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
29.12.2015
Cell Press Elsevier |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Targeted therapies designed to exploit specific molecular pathways in aggressive cancers are an exciting area of current research. Mixed Lineage Leukemia (MLL) mutations such as the t(4;11) translocation cause aggressive leukemias that are refractory to conventional treatment. The t(4;11) translocation produces an MLL/AF4 fusion protein that activates key target genes through both epigenetic and transcriptional elongation mechanisms. In this study, we show that t(4;11) patient cells express high levels of BCL-2 and are highly sensitive to treatment with the BCL-2-specific BH3 mimetic ABT-199. We demonstrate that MLL/AF4 specifically upregulates the BCL-2 gene but not other BCL-2 family members via DOT1L-mediated H3K79me2/3. We use this information to show that a t(4;11) cell line is sensitive to a combination of ABT-199 and DOT1L inhibitors. In addition, ABT-199 synergizes with standard induction-type therapy in a xenotransplant model, advocating for the introduction of ABT-199 into therapeutic regimens for MLL-rearranged leukemias.
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•MLLr ALL blasts express high levels of BCL-2, BAX, and BIM•MLL/AF4 activates BCL2 through H3K79 methylation•MLLr ALL cells are exquisitely sensitive to BCL-2 antagonist ABT-199•ABT-199 treatment synergizes with H3K79 methylation inhibitors on MLLr samples
Therapies designed to exploit specific molecular pathways in aggressive cancers are an exciting area of research. Mutations in the MLL gene cause aggressive incurable leukemias. Benito et al. show that MLL leukemias are highly sensitive to BCL-2 inhibitors, especially when combined with drugs that target mutant MLL complex activity. |
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| AbstractList | Targeted therapies designed to exploit specific molecular pathways in aggressive cancers are an exciting area of current research. Mixed Lineage Leukemia (MLL) mutations such as the t(4;11) translocation cause aggressive leukemias that are refractory to conventional treatment. The t(4;11) translocation produces an MLL/AF4 fusion protein that activates key target genes through both epigenetic and transcriptional elongation mechanisms. In this study, we show that t(4;11) patient cells express high levels of BCL-2 and are highly sensitive to treatment with the BCL-2-specific BH3 mimetic ABT-199. We demonstrate that MLL/AF4 specifically upregulates the BCL-2 gene but not other BCL-2 family members via DOT1L-mediated H3K79me2/3. We use this information to show that a t(4;11) cell line is sensitive to a combination of ABT-199 and DOT1L inhibitors. In addition, ABT-199 synergizes with standard induction-type therapy in a xenotransplant model, advocating for the introduction of ABT-199 into therapeutic regimens for MLL-rearranged leukemias. Targeted therapies designed to exploit specific molecular pathways in aggressive cancers are an exciting area of current research. Mixed Lineage Leukemia (MLL) mutations such as the t(4;11) translocation cause aggressive leukemias that are refractory to conventional treatment. The t(4;11) translocation produces an MLL/AF4 fusion protein that activates key target genes through both epigenetic and transcriptional elongation mechanisms. In this study, we show that t(4;11) patient cells express high levels of BCL-2 and are highly sensitive to treatment with the BCL-2-specific BH3 mimetic ABT-199. We demonstrate that MLL/AF4 specifically upregulates the BCL-2 gene but not other BCL-2 family members via DOT1L-mediated H3K79me2/3. We use this information to show that a t(4;11) cell line is sensitive to a combination of ABT-199 and DOT1L inhibitors. In addition, ABT-199 synergizes with standard induction-type therapy in a xenotransplant model, advocating for the introduction of ABT-199 into therapeutic regimens for MLL-rearranged leukemias. [Display omitted] •MLLr ALL blasts express high levels of BCL-2, BAX, and BIM•MLL/AF4 activates BCL2 through H3K79 methylation•MLLr ALL cells are exquisitely sensitive to BCL-2 antagonist ABT-199•ABT-199 treatment synergizes with H3K79 methylation inhibitors on MLLr samples Therapies designed to exploit specific molecular pathways in aggressive cancers are an exciting area of research. Mutations in the MLL gene cause aggressive incurable leukemias. Benito et al. show that MLL leukemias are highly sensitive to BCL-2 inhibitors, especially when combined with drugs that target mutant MLL complex activity. Targeted therapies designed to exploit specific molecular pathways in aggressive cancers are an exciting area of current research. Mixed Lineage Leukemia ( MLL ) mutations such as the t(4;11) translocation cause aggressive leukemias that are refractory to conventional treatment. The t(4;11) translocation produces an MLL/AF4 fusion protein that activates key target genes through both epigenetic and transcriptional elongation mechanisms. In this study, we show that t(4;11) patient cells express high levels of BCL-2 and are highly sensitive to treatment with the BCL-2-specific BH3 mimetic ABT-199. We demonstrate that MLL/AF4 specifically upregulates the BCL-2 gene but not other BCL-2 family members via DOT1L-mediated H3K79me2/3. We use this information to show that a t(4;11) cell line is sensitive to a combination of ABT-199 and DOT1L inhibitors. In addition, ABT-199 synergizes with standard induction-type therapy in a xenotransplant model, advocating for the introduction of ABT-199 into therapeutic regimens for MLL-rearranged leukemias. • MLLr ALL blasts express high levels of BCL-2, BAX, and BIM • MLL/AF4 activates BCL2 through H3K79 methylation • MLLr ALL cells are exquisitely sensitive to BCL-2 antagonist ABT-199 • ABT-199 treatment synergizes with H3K79 methylation inhibitors on MLLr samples Therapies designed to exploit specific molecular pathways in aggressive cancers are an exciting area of research. Mutations in the MLL gene cause aggressive incurable leukemias. Benito et al. show that MLL leukemias are highly sensitive to BCL-2 inhibitors, especially when combined with drugs that target mutant MLL complex activity. |
| Author | Zhou, Ping Coombes, Kevin R. Müschen, Markus Mulloy, James C. Ma, Helen Wunderlich, Mark Qiu, Yihua Harutyunyan, Karine G. Kerry, Jon Milne, Thomas A. Thomas, Deborah A. Andreeff, Michael Letai, Anthony Godfrey, Laura Jeremias, Irmela Zweidler-McKay, Patrick A. Konopleva, Marina Debose, LaKiesha Jacamo, Rodrigo Kantarjian, Hagop M. Zhang, Nianxiang Golfman, Leonard Benito, Juliana M. Geng, Huimin Marzo, Isabel Hogdal, Leah O’Brien, Susan Park, Eugene Kojima, Kensuke Kornblau, Steven M. Gonzalo, Oscar Ballabio, Erica Chonghaile, Triona Ní North, Phillip Leverson, Joel D. O’Brien, Eric |
| AuthorAffiliation | 5 Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA 8 Division of Pediatrics, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA 10 German Research Center for Environmental Health (GmbH), 85764 Neuherberg, Germany 6 Department of Laboratory Medicine, University of California, San Francisco, San Francisco, CA 94143, USA 9 Department of Physiology and Medical Physics, Royal College of Surgeons in Ireland, York House, Dublin 2, Ireland 3 Division of Hematology, Respiratory Medicine and Oncology, Department of Internal Medicine, Faculty of Medicine, Saga University, Saga 840-8502, Japan 4 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA 2 Weatherall Institute of Molecular Medicine, Molecular Haematology Unit, NIHR Oxford Biomedical Research Centre Programme, University of Oxford, Headington, Oxford OX3 9DS, UK 7 Department of Biochemistry, Molecular and Cell Biology, University of |
| AuthorAffiliation_xml | – name: 2 Weatherall Institute of Molecular Medicine, Molecular Haematology Unit, NIHR Oxford Biomedical Research Centre Programme, University of Oxford, Headington, Oxford OX3 9DS, UK – name: 5 Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA – name: 11 Department of Bioinformatics and Computational Biology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – name: 9 Department of Physiology and Medical Physics, Royal College of Surgeons in Ireland, York House, Dublin 2, Ireland – name: 7 Department of Biochemistry, Molecular and Cell Biology, University of Zaragoza, 50018 Zaragoza, Spain – name: 12 Department of Oncology Development, AbbVie Inc., North Chicago, IL 60064, USA – name: 1 Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – name: 3 Division of Hematology, Respiratory Medicine and Oncology, Department of Internal Medicine, Faculty of Medicine, Saga University, Saga 840-8502, Japan – name: 4 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA – name: 10 German Research Center for Environmental Health (GmbH), 85764 Neuherberg, Germany – name: 6 Department of Laboratory Medicine, University of California, San Francisco, San Francisco, CA 94143, USA – name: 8 Division of Pediatrics, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA |
| Author_xml | – sequence: 1 givenname: Juliana M. surname: Benito fullname: Benito, Juliana M. organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 2 givenname: Laura surname: Godfrey fullname: Godfrey, Laura organization: Weatherall Institute of Molecular Medicine, Molecular Haematology Unit, NIHR Oxford Biomedical Research Centre Programme, University of Oxford, Headington, Oxford OX3 9DS, UK – sequence: 3 givenname: Kensuke surname: Kojima fullname: Kojima, Kensuke organization: Division of Hematology, Respiratory Medicine and Oncology, Department of Internal Medicine, Faculty of Medicine, Saga University, Saga 840-8502, Japan – sequence: 4 givenname: Leah surname: Hogdal fullname: Hogdal, Leah organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA – sequence: 5 givenname: Mark surname: Wunderlich fullname: Wunderlich, Mark organization: Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA – sequence: 6 givenname: Huimin surname: Geng fullname: Geng, Huimin organization: Department of Laboratory Medicine, University of California, San Francisco, San Francisco, CA 94143, USA – sequence: 7 givenname: Isabel surname: Marzo fullname: Marzo, Isabel organization: Department of Biochemistry, Molecular and Cell Biology, University of Zaragoza, 50018 Zaragoza, Spain – sequence: 8 givenname: Karine G. surname: Harutyunyan fullname: Harutyunyan, Karine G. organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 9 givenname: Leonard surname: Golfman fullname: Golfman, Leonard organization: Division of Pediatrics, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 10 givenname: Phillip surname: North fullname: North, Phillip organization: Weatherall Institute of Molecular Medicine, Molecular 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University of Zaragoza, 50018 Zaragoza, Spain – sequence: 15 givenname: Yihua surname: Qiu fullname: Qiu, Yihua organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 16 givenname: Irmela surname: Jeremias fullname: Jeremias, Irmela organization: German Research Center for Environmental Health (GmbH), 85764 Neuherberg, Germany – sequence: 17 givenname: LaKiesha surname: Debose fullname: Debose, LaKiesha organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 18 givenname: Eric surname: O’Brien fullname: O’Brien, Eric organization: Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA – sequence: 19 givenname: Helen surname: Ma fullname: Ma, Helen organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 20 givenname: Ping surname: Zhou fullname: Zhou, Ping organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 21 givenname: Rodrigo surname: Jacamo fullname: Jacamo, Rodrigo organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 22 givenname: Eugene surname: Park fullname: Park, Eugene organization: Department of Laboratory Medicine, University of California, San Francisco, San Francisco, CA 94143, USA – sequence: 23 givenname: Kevin R. surname: Coombes fullname: Coombes, Kevin R. organization: Department of Bioinformatics and Computational Biology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 24 givenname: Nianxiang surname: Zhang fullname: Zhang, Nianxiang organization: Department of Bioinformatics and Computational Biology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 25 givenname: Deborah A. surname: Thomas fullname: Thomas, Deborah A. organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 26 givenname: Susan surname: O’Brien fullname: O’Brien, Susan organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 27 givenname: Hagop M. surname: Kantarjian fullname: Kantarjian, Hagop M. organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 28 givenname: Joel D. surname: Leverson fullname: Leverson, Joel D. organization: Department of Oncology Development, AbbVie Inc., North Chicago, IL 60064, USA – sequence: 29 givenname: Steven M. surname: Kornblau fullname: Kornblau, Steven M. organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 30 givenname: Michael surname: Andreeff fullname: Andreeff, Michael organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 31 givenname: Markus surname: Müschen fullname: Müschen, Markus organization: Department of Laboratory Medicine, University of California, San Francisco, San Francisco, CA 94143, USA – sequence: 32 givenname: Patrick A. surname: Zweidler-McKay fullname: Zweidler-McKay, Patrick A. organization: Division of Pediatrics, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 33 givenname: James C. surname: Mulloy fullname: Mulloy, James C. organization: Cancer and Blood Diseases Institute, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA – sequence: 34 givenname: Anthony surname: Letai fullname: Letai, Anthony organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA – sequence: 35 givenname: Thomas A. surname: Milne fullname: Milne, Thomas A. email: thomas.milne@imm.ox.ac.uk organization: Weatherall Institute of Molecular Medicine, Molecular Haematology Unit, NIHR Oxford Biomedical Research Centre Programme, University of Oxford, Headington, Oxford OX3 9DS, UK – sequence: 36 givenname: Marina surname: Konopleva fullname: Konopleva, Marina email: mkonople@mdanderson.org organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26711339$$D View this record in MEDLINE/PubMed |
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| IngestDate | Tue Oct 22 15:15:53 EDT 2024 Tue Sep 17 21:26:23 EDT 2024 Thu Sep 26 19:08:56 EDT 2024 Sat Nov 02 12:23:40 EDT 2024 Wed May 17 01:06:27 EDT 2023 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 12 |
| Keywords | MLL/AF4 apoptosis pathways bcl-2 family members leukemias H3K79 methylation DOT1L |
| Language | English |
| License | http://creativecommons.org/licenses/by/4.0 Copyright © 2015 The Authors. Published by Elsevier Inc. All rights reserved. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
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| OpenAccessLink | https://doaj.org/article/c1a105f3ea7b4ced908a81b1bad07bcd |
| PMID | 26711339 |
| PageCount | 13 |
| ParticipantIDs | doaj_primary_oai_doaj_org_article_c1a105f3ea7b4ced908a81b1bad07bcd pubmedcentral_primary_oai_pubmedcentral_nih_gov_4700051 crossref_primary_10_1016_j_celrep_2015_12_003 pubmed_primary_26711339 elsevier_sciencedirect_doi_10_1016_j_celrep_2015_12_003 |
| PublicationCentury | 2000 |
| PublicationDate | 2015-12-29 |
| PublicationDateYYYYMMDD | 2015-12-29 |
| PublicationDate_xml | – month: 12 year: 2015 text: 2015-12-29 day: 29 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States |
| PublicationTitle | Cell reports (Cambridge) |
| PublicationTitleAlternate | Cell Rep |
| PublicationYear | 2015 |
| Publisher | Elsevier Inc Cell Press Elsevier |
| Publisher_xml | – name: Elsevier Inc – name: Cell Press – name: Elsevier |
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| Snippet | Targeted therapies designed to exploit specific molecular pathways in aggressive cancers are an exciting area of current research. Mixed Lineage Leukemia (MLL)... Targeted therapies designed to exploit specific molecular pathways in aggressive cancers are an exciting area of current research. Mixed Lineage Leukemia ( MLL... |
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| SubjectTerms | Animals apoptosis pathways bcl-2 family members Bridged Bicyclo Compounds, Heterocyclic - pharmacology Cell Line, Tumor DOT1L Genes, bcl-2 H3K79 methylation Histone-Lysine N-Methyltransferase - genetics Humans leukemias Methylation Mice Mice, Inbred NOD Mice, SCID MLL/AF4 Myeloid-Lymphoid Leukemia Protein - genetics Myeloid-Lymphoid Leukemia Protein - metabolism Precursor B-Cell Lymphoblastic Leukemia-Lymphoma - drug therapy Precursor B-Cell Lymphoblastic Leukemia-Lymphoma - genetics Precursor B-Cell Lymphoblastic Leukemia-Lymphoma - metabolism Proto-Oncogene Proteins c-bcl-2 - antagonists & inhibitors Proto-Oncogene Proteins c-bcl-2 - genetics Proto-Oncogene Proteins c-bcl-2 - metabolism Sulfonamides - pharmacology |
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| Title | MLL-Rearranged Acute Lymphoblastic Leukemias Activate BCL-2 through H3K79 Methylation and Are Sensitive to the BCL-2-Specific Antagonist ABT-199 |
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