Targeting transcription regulation in cancer with a covalent CDK7 inhibitor
Here, a covalent inhibitor targeting cyclin-dependent kinase 7 (CDK7) demonstrates in vitro and in vivo efficacy against T-cell acute lymphoblastic leukaemia by downregulating oncogenic transcriptional programs. CDK7 kinase as an anti-cancer target Pharmacological blockade of transcription is a poss...
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Published in | Nature (London) Vol. 511; no. 7511; pp. 616 - 620 |
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Main Authors | , , , , , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
31.07.2014
Nature Publishing Group |
Subjects | |
Online Access | Get full text |
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Abstract | Here, a covalent inhibitor targeting cyclin-dependent kinase 7 (CDK7) demonstrates
in vitro
and
in vivo
efficacy against T-cell acute lymphoblastic leukaemia by downregulating oncogenic transcriptional programs.
CDK7 kinase as an anti-cancer target
Pharmacological blockade of transcription is a possible means of targeting cancer cells. Direct pharmacological inhibition of transcription factors has proved problematic, so cyclin-dependent kinase (CDK) family members such as CDK7, which regulate transcription by phosphorylating the carboxy-terminal domain of RNA polymerase II, could provide more druggable targets. Here Nathanael Gray and colleagues use a cell-based screen to identify a novel transcriptional inhibitor, THZ1, that covalently targets CDK7 and has anti-proliferative activity in human T-cell acute lymphoblastic leukaemia cell lines and in a xenograft mouse model. THZ1 is a phenylaminopyrimidine that uses a mechanism combining ATP-site and allosteric covalent binding as a means of attaining potency and selectivity for CDK7.
Tumour oncogenes include transcription factors that co-opt the general transcriptional machinery to sustain the oncogenic state
1
, but direct pharmacological inhibition of transcription factors has so far proven difficult
2
. However, the transcriptional machinery contains various enzymatic cofactors that can be targeted for the development of new therapeutic candidates
3
, including cyclin-dependent kinases (CDKs)
4
. Here we present the discovery and characterization of a covalent CDK7 inhibitor, THZ1, which has the unprecedented ability to target a remote cysteine residue located outside of the canonical kinase domain, providing an unanticipated means of achieving selectivity for CDK7. Cancer cell-line profiling indicates that a subset of cancer cell lines, including human T-cell acute lymphoblastic leukaemia (T-ALL), have exceptional sensitivity to THZ1. Genome-wide analysis in Jurkat T-ALL cells shows that THZ1 disproportionally affects transcription of
RUNX1
and suggests that sensitivity to THZ1 may be due to vulnerability conferred by the
RUNX1
super-enhancer and the key role of
RUNX1
in the core transcriptional regulatory circuitry of these tumour cells. Pharmacological modulation of CDK7 kinase activity may thus provide an approach to identify and treat tumour types that are dependent on transcription for maintenance of the oncogenic state. |
---|---|
AbstractList | Tumor oncogenes include transcription factors that co-opt the general transcriptional machinery to sustain the oncogenic state
1
, but direct pharmacological inhibition of transcription factors has thus far proven difficult
2
. However, the transcriptional machinery contains various enzymatic co-factors that can be targeted for development of new therapeutic candidates
3
, including cyclin-dependent kinases (CDKs)
4
. Here we present the discovery and characterization of the first covalent CDK7 inhibitor, THZ1, which has the unprecedented ability to target a remote cysteine residue located outside of the canonical kinase domain, providing an unanticipated means of achieving selectivity for CDK7. Cancer cell line profiling indicates that a subset of cancer cell lines, including T-ALL, exhibit exceptional sensitivity to THZ1. Genome-wide analysis in Jurkat T-ALL shows that THZ1 disproportionally affects transcription of
RUNX1
and suggests that sensitivity to THZ1 may be due to vulnerability conferred by the
RUNX1
super-enhancer and this transcription factor’s key role in the core transcriptional regulatory circuitry of these tumor cells. Pharmacological modulation of CDK7 kinase activity may thus provide an approach to identify and treat tumor types exhibiting extreme dependencies on transcription for maintenance of the oncogenic state. Tumour oncogenes include transcription factors that co-opt the general transcriptional machinery to sustain the oncogenic state (1), but direct pharmacological inhibition of transcription factors has so far proven difficult (2). However, the transcriptional machinery contains various enzymatic cofactors that can be targeted for the development of new therapeutic candidates (3), including cyclin-dependent kinases (CDKs) (4). Here we present the discovery and characterization of a covalent CDK7 inhibitor, THZ1, which has the unprecedented ability to target a remote cysteine residue located outside of the canonical kinase domain, providing an unanticipated means of achieving selectivity for CDK7. Cancer cell-line profiling indicates that a subset of cancer cell lines, including human T-cell acute lymphoblastic leukaemia (T-ALL), have exceptional sensitivity to THZ1. Genome-wide analysis in Jurkat T-ALL cells shows that THZ1 disproportionally affects transcription of RUNX1 and suggests that sensitivity to THZ1 may be due to vulnerability conferred by the RUNX1 super-enhancer and the key role of RUNX1 in the core transcriptional regulatory circuitry of these tumour cells. Pharmacological modulation of CDK7 kinase activity may thus provide an approach to identify and treat tumour types that are dependent on transcription for maintenance of the oncogenic state. Tumour oncogenes include transcription factors that co-opt the general transcriptional machinery to sustain the oncogenic state, but direct pharmacological inhibition of transcription factors has so far proven difficult. However, the transcriptional machinery contains various enzymatic cofactors that can be targeted for the development of new therapeutic candidates, including cyclin-dependent kinases (CDKs). Here we present the discovery and characterization of a covalent CDK7 inhibitor, THZ1, which has the unprecedented ability to target a remote cysteine residue located outside of the canonical kinase domain, providing an unanticipated means of achieving selectivity for CDK7. Cancer cell-line profiling indicates that a subset of cancer cell lines, including human T-cell acute lymphoblastic leukaemia (T-ALL), have exceptional sensitivity to THZ1. Genome-wide analysis in Jurkat T-ALL cells shows that THZ1 disproportionally affects transcription of RUNX1 and suggests that sensitivity to THZ1 may be due to vulnerability conferred by the RUNX1 super-enhancer and the key role of RUNX1 in the core transcriptional regulatory circuitry of these tumour cells. Pharmacological modulation of CDK7 kinase activity may thus provide an approach to identify and treat tumour types that are dependent on transcription for maintenance of the oncogenic state. Tumour oncogenes include transcription factors that co-opt the general transcriptional machinery to sustain the oncogenic state, but direct pharmacological inhibition of transcription factors has so far proven difficult. However, the transcriptional machinery contains various enzymatic cofactors that can be targeted for the development of new therapeutic candidates, including cyclin-dependent kinases (CDKs). Here we present the discovery and characterization of a covalent CDK7 inhibitor,THZ1, which has the unprecedented ability to target a remote cysteine residue located outside of the canonical kinase domain, providing an unanticipated means of achieving selectivity for CDK7. Cancer cell-line profiling indicates that a subset of cancer cell lines, including human T-cell acute lymphoblastic leukaemia (T-ALL), have exceptional sensitivity to THZ1. Genome-wide analysis in Jurkat T-ALL cells shows that THZ1disproportionally affects transcription of RUNX1 and suggests that sensitivity toTHZ1 may be due to vulnerability conferred by the RUNX1 super-enhancer and the key role of RUNX1 in the core transcriptional regulatory circuitry of these tumour cells. Pharmacological modulation of CDK7 kinase activity may thus provide an approach to identify and treat tumour types that are dependent on transcription for maintenance of the oncogenic state. Here, a covalent inhibitor targeting cyclin-dependent kinase 7 (CDK7) demonstrates in vitro and in vivo efficacy against T-cell acute lymphoblastic leukaemia by downregulating oncogenic transcriptional programs. CDK7 kinase as an anti-cancer target Pharmacological blockade of transcription is a possible means of targeting cancer cells. Direct pharmacological inhibition of transcription factors has proved problematic, so cyclin-dependent kinase (CDK) family members such as CDK7, which regulate transcription by phosphorylating the carboxy-terminal domain of RNA polymerase II, could provide more druggable targets. Here Nathanael Gray and colleagues use a cell-based screen to identify a novel transcriptional inhibitor, THZ1, that covalently targets CDK7 and has anti-proliferative activity in human T-cell acute lymphoblastic leukaemia cell lines and in a xenograft mouse model. THZ1 is a phenylaminopyrimidine that uses a mechanism combining ATP-site and allosteric covalent binding as a means of attaining potency and selectivity for CDK7. Tumour oncogenes include transcription factors that co-opt the general transcriptional machinery to sustain the oncogenic state 1 , but direct pharmacological inhibition of transcription factors has so far proven difficult 2 . However, the transcriptional machinery contains various enzymatic cofactors that can be targeted for the development of new therapeutic candidates 3 , including cyclin-dependent kinases (CDKs) 4 . Here we present the discovery and characterization of a covalent CDK7 inhibitor, THZ1, which has the unprecedented ability to target a remote cysteine residue located outside of the canonical kinase domain, providing an unanticipated means of achieving selectivity for CDK7. Cancer cell-line profiling indicates that a subset of cancer cell lines, including human T-cell acute lymphoblastic leukaemia (T-ALL), have exceptional sensitivity to THZ1. Genome-wide analysis in Jurkat T-ALL cells shows that THZ1 disproportionally affects transcription of RUNX1 and suggests that sensitivity to THZ1 may be due to vulnerability conferred by the RUNX1 super-enhancer and the key role of RUNX1 in the core transcriptional regulatory circuitry of these tumour cells. Pharmacological modulation of CDK7 kinase activity may thus provide an approach to identify and treat tumour types that are dependent on transcription for maintenance of the oncogenic state. |
Audience | Academic |
Author | Sim, Taebo Mitsiades, Constantine S. Young, Richard A. Weng, Andrew P. Hannett, Nancy M. Marto, Jarrod A. Gray, Nathanael S. Rahl, Peter B. Kwiatkowski, Nicholas Abraham, Brian J. Ficarro, Scott B. Brown, Jennifer R. Sanda, Takaomi Look, Thomas McMillin, Douglas Dastur, Anahita Reddy, Jessica Benes, Cyril H. Amzallag, Arnaud Ramaswamy, Sridhar Jenkins, Catherine E. Kim, Nam Doo Zhang, Tinghu Tesar, Bethany |
AuthorAffiliation | 4 Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA 7 Broad Institute of MIT and Harvard, 7 Cambridge Center, Cambridge, MA 02142, USA 12 Cancer Science Institute of Singapore, National University of Singapore, Singapore 117599 6 Department of Medicine Massachusetts General Hospital Cancer Center and Harvard Medical School, Charlestown, MA 02129, USA 10 Terry Fox Laboratory, British Columbia Cancer Agency, Vancouver, British Columbia, Canada 18 Division of Hematology/Oncology, Children’s Hospital, Boston, MA 02115 USA 2 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA 8 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02115, USA 14 Daegu-Gyeongbuk Medical Innovation Foundation, 2387 dalgubeol-daero, Suseong-gu, Daegu, 706-010, Korea 3 Whitehead Institute for Biomedical Research, 9 Cambridge Center, Cambridge, MA 02142, USA 9 Department of Medicine, Brig |
AuthorAffiliation_xml | – name: 2 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA – name: 3 Whitehead Institute for Biomedical Research, 9 Cambridge Center, Cambridge, MA 02142, USA – name: 10 Terry Fox Laboratory, British Columbia Cancer Agency, Vancouver, British Columbia, Canada – name: 11 Department of Pediatric Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – name: 14 Daegu-Gyeongbuk Medical Innovation Foundation, 2387 dalgubeol-daero, Suseong-gu, Daegu, 706-010, Korea – name: 7 Broad Institute of MIT and Harvard, 7 Cambridge Center, Cambridge, MA 02142, USA – name: 9 Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA – name: 12 Cancer Science Institute of Singapore, National University of Singapore, Singapore 117599 – name: 5 Blais Proteomics Center, Dana-Farber Cancer Institute, Boston, MA 02115, USA – name: 8 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02115, USA – name: 13 Chemical Kinomics Research Center, Korea Institute of Science and Technology, 39-1, Hawolgok-dong, Seongbuk-gu, Seoul, 136-791, Korea/ KU-KIST Graduate School of Converging Science and Technology, 145, Anam-ro, Seoul, Korea – name: 4 Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA – name: 6 Department of Medicine Massachusetts General Hospital Cancer Center and Harvard Medical School, Charlestown, MA 02129, USA – name: 18 Division of Hematology/Oncology, Children’s Hospital, Boston, MA 02115 USA – name: 1 Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02115, USA |
Author_xml | – sequence: 1 givenname: Nicholas surname: Kwiatkowski fullname: Kwiatkowski, Nicholas organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Whitehead Institute for Biomedical Research, 9 Cambridge Center – sequence: 2 givenname: Tinghu surname: Zhang fullname: Zhang, Tinghu organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School – sequence: 3 givenname: Peter B. surname: Rahl fullname: Rahl, Peter B. organization: Whitehead Institute for Biomedical Research, 9 Cambridge Center – sequence: 4 givenname: Brian J. surname: Abraham fullname: Abraham, Brian J. organization: Whitehead Institute for Biomedical Research, 9 Cambridge Center – sequence: 5 givenname: Jessica surname: Reddy fullname: Reddy, Jessica organization: Whitehead Institute for Biomedical Research, 9 Cambridge Center, Department of Biology, Massachusetts Institute of Technology – sequence: 6 givenname: Scott B. surname: Ficarro fullname: Ficarro, Scott B. organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Blais Proteomics Center, Dana-Farber Cancer Institute – sequence: 7 givenname: Anahita surname: Dastur fullname: Dastur, Anahita organization: Department of Medicine Massachusetts General Hospital Cancer Center and Harvard Medical School – sequence: 8 givenname: Arnaud surname: Amzallag fullname: Amzallag, Arnaud organization: Department of Medicine Massachusetts General Hospital Cancer Center and Harvard Medical School, Broad Institute of MIT and Harvard, 7 Cambridge Center – sequence: 9 givenname: Sridhar surname: Ramaswamy fullname: Ramaswamy, Sridhar organization: Department of Medicine Massachusetts General Hospital Cancer Center and Harvard Medical School, Broad Institute of MIT and Harvard, 7 Cambridge Center – sequence: 10 givenname: Bethany surname: Tesar fullname: Tesar, Bethany organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School – sequence: 11 givenname: Catherine E. surname: Jenkins fullname: Jenkins, Catherine E. organization: Terry Fox Laboratory, British Columbia Cancer Agency, Vancouver, British Columbia V5Z 1L3, Canada – sequence: 12 givenname: Nancy M. surname: Hannett fullname: Hannett, Nancy M. organization: Whitehead Institute for Biomedical Research, 9 Cambridge Center – sequence: 13 givenname: Douglas surname: McMillin fullname: McMillin, Douglas organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School – sequence: 14 givenname: Takaomi surname: Sanda fullname: Sanda, Takaomi organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Cancer Science Institute of Singapore, National University of Singapore, 117599 Singapore – sequence: 15 givenname: Taebo surname: Sim fullname: Sim, Taebo organization: Chemical Kinomics Research Center, Korea Institute of Science and Technology, 39-1, Hawolgok-dong, Seongbuk-gu, Seoul 136-791, Korea, and KU-KIST Graduate School of Converging Science and Technology, 145, Anam-ro, Seongbuk-gu, Seoul 136-713, Korea – sequence: 16 givenname: Nam Doo surname: Kim fullname: Kim, Nam Doo organization: Daegu-Gyeongbuk Medical Innovation Foundation, 2387 dalgubeol-daero, Suseong-gu, Daegu 706-010, Korea – sequence: 17 givenname: Thomas surname: Look fullname: Look, Thomas organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Division of Hematology/Oncology, Children’s Hospital – sequence: 18 givenname: Constantine S. surname: Mitsiades fullname: Mitsiades, Constantine S. organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School – sequence: 19 givenname: Andrew P. surname: Weng fullname: Weng, Andrew P. organization: Terry Fox Laboratory, British Columbia Cancer Agency, Vancouver, British Columbia V5Z 1L3, Canada – sequence: 20 givenname: Jennifer R. surname: Brown fullname: Brown, Jennifer R. organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School – sequence: 21 givenname: Cyril H. surname: Benes fullname: Benes, Cyril H. organization: Department of Medicine Massachusetts General Hospital Cancer Center and Harvard Medical School – sequence: 22 givenname: Jarrod A. surname: Marto fullname: Marto, Jarrod A. organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Blais Proteomics Center, Dana-Farber Cancer Institute – sequence: 23 givenname: Richard A. surname: Young fullname: Young, Richard A. email: young@wi.mit.edu organization: Whitehead Institute for Biomedical Research, 9 Cambridge Center, Department of Biology, Massachusetts Institute of Technology – sequence: 24 givenname: Nathanael S. surname: Gray fullname: Gray, Nathanael S. email: nathanael_gray@dfci.harvard.edu organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25043025$$D View this record in MEDLINE/PubMed |
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Snippet | Here, a covalent inhibitor targeting cyclin-dependent kinase 7 (CDK7) demonstrates
in vitro
and
in vivo
efficacy against T-cell acute lymphoblastic leukaemia... Tumour oncogenes include transcription factors that co-opt the general transcriptional machinery to sustain the oncogenic state, but direct pharmacological... Tumour oncogenes include transcription factors that co-opt the general transcriptional machinery to sustain the oncogenic state (1), but direct pharmacological... Tumor oncogenes include transcription factors that co-opt the general transcriptional machinery to sustain the oncogenic state 1 , but direct pharmacological... |
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SubjectTerms | 38/61 45/15 59/5 631/154/555 631/67/1990/283 631/67/395 631/92/275 82/58 96/2 96/31 96/98 Analysis Antineoplastic Agents - pharmacology Cancer Care and treatment Cell Line, Tumor Cell Proliferation - drug effects Cell Survival - drug effects Core Binding Factor Alpha 2 Subunit - metabolism Crystal structure Cyclin-Dependent Kinases - antagonists & inhibitors Cysteine Cysteine - metabolism Enzyme Inhibitors - pharmacology Experiments Gene expression Gene Expression Regulation, Neoplastic - drug effects Genetic aspects Genetic regulation Genetic transcription Health aspects Humanities and Social Sciences Humans Jurkat Cells Kinases letter Leukemia multidisciplinary Pharmacology Phenylenediamines - pharmacology Phosphorylation Phosphorylation - drug effects Precursor T-Cell Lymphoblastic Leukemia-Lymphoma - enzymology Pyrimidines - pharmacology Regression analysis Science Transcription factors |
Title | Targeting transcription regulation in cancer with a covalent CDK7 inhibitor |
URI | https://link.springer.com/article/10.1038/nature13393 https://www.ncbi.nlm.nih.gov/pubmed/25043025 https://www.proquest.com/docview/1551986268 https://pubmed.ncbi.nlm.nih.gov/PMC4244910 |
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