Pharmacological targeting of the Wdr5-MLL interaction in C/EBPα N-terminal leukemia

Nature Chemical Biology - Tập 11 Số 8 - Trang 571-578 - 2015
Florian Grebien1, Masoud Vedadi2, Matthäus Getlik3, Roberto Giambruno1, Amit Grover4, Roberto Avellino5, Anna Skucha1, Sarah Vittori1, Ekaterina Kuznetsova2, David Smil2, Dalia Baršytė-Lovejoy2, Fengling Li2, Gennadiy Poda3, Matthieu Schapira2, Hong Wu2, Aiping Dong2, Guillermo Senisterra2, Alexey Stukalov1, K. Huber1, Andreas Schönegger1, Richard Marcellus3, Martin Bilban6, Christoph Bock1, Peter J. Brown2, Johannes Zuber7, Keiryn L. Bennett1, Rima Al‐awar8, Ruud Delwel5, Claus Nerlov4, C.H. Arrowsmith9, Giulio Superti‐Furga10
1CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria
2Structural Genomics Consortium, University of Toronto, Toronto, Ontario, Canada.
3Drug Discovery Program, Ontario Institute for Cancer Research, Toronto, Ontario, Canada
4MRC Molecular Hematology Unit, Weatherall Institute of Molecular Medicine, Oxford, UK
5Department of Hematology, Erasmus University Medical Center, Rotterdam, The Netherlands;
6Department of Laboratory Medicine and Core Facility Genomics, Core Facilities, Medical University Vienna, Vienna, Austria
7Research Institute of Molecular Pathology, Vienna, Austria
8Department of Pharmacology and Toxicology, University of Toronto, Toronto, Ontario, Canada
9Princess Margaret Cancer Centre, Toronto, Ontario, Canada
10Center for Physiology and Pharmacology, Medical University Vienna, Vienna, Austria

Tóm tắt

Từ khóa


Tài liệu tham khảo

Koschmieder, S., Halmos, B., Levantini, E. & Tenen, D.G. Dysregulation of the C/EBPα differentiation pathway in human cancer. J. Clin. Oncol. 27, 619–628 (2009).

Zhang, P. et al. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBPα. Immunity 21, 853–863 (2004).

Leroy, H. et al. CEBPA point mutations in hematological malignancies. Leukemia 19, 329–334 (2005).

Fasan, A. et al. The role of different genetic subtypes of CEBPA mutated AML. Leukemia 28, 794–803 (2014).

Nerlov, C. C/EBPα mutations in acute myeloid leukaemias. Nat. Rev. Cancer 4, 394–400 (2004).

Kirstetter, P. et al. Modeling of C/EBPα mutant acute myeloid leukemia reveals a common expression signature of committed myeloid leukemia-initiating cells. Cancer Cell 13, 299–310 (2008).

Friedman, A.D. & McKnight, S. Identification of two polypeptide segments of CCAAT/enhancer-binding protein required for transcriptional activation of the serum albumin gene. Genes Dev. 4, 1416–1426 (1990).

Nerlov, C. & Ziff, E.B. Three levels of functional interaction determine the activity of CCAAT/enhancer binding protein-α on the serum albumin promoter. Genes Dev. 8, 350–362 (1994).

Pedersen, T.A., Kowenz-Leutz, E., Leutz, A. & Nerlov, C. Cooperation between C/EBPα TBP/TFIIB and SWI/SNF recruiting domains is required for adipocyte differentiation. Genes Dev. 15, 3208–3216 (2001).

Slomiany, B.A., Arigo, K.L.D., Kelly, M.M. & Kurtz, D.T. C/EBPα inhibits cell growth via direct repression of E2F-DP–mediated transcription. Mol. Cell. Biol. 20, 5986–5997 (2000).

Porse, B.T. et al. E2F repression by C/EBPα is required for adipogenesis and granulopoiesis in vivo. Cell 107, 247–258 (2001).

D'Alo', F. et al. The amino terminal and E2F interaction domains are critical for C/EBPα–mediated induction of granulopoietic development of hematopoietic cells. Blood 102, 3163–3171 (2003).

Wang, Q.-F., Cleaves, R., Kummalue, T., Nerlov, C. & Friedman, A.D. Cell cycle inhibition mediated by the outer surface of the C/EBPα basic region is required but not sufficient for granulopoiesis. Oncogene 22, 2548–2557 (2003).

Cleaves, R., Wang, Q. & Friedman, A.D. C/EBPα p30, a myeloid leukemia oncoprotein, limits G-CSF receptor expression but not terminal granulopoiesis via site-selective inhibition of C/EBP DNA binding. Oncogene 23, 716–725 (2004).

Zada, A.A. et al. Proteomic discovery of Max as a novel interacting partner of C/EBPα: a Myc/Max/Mad link. Leukemia 20, 2137–2146 (2006).

Trivedi, A.K. et al. Proteomic identification of C/EBP-DBD multiprotein complex: JNK1 activates stem cell regulator C/EBPα by inhibiting its ubiquitination. Oncogene 26, 1789–1801 (2007).

Bararia, D. et al. Proteomic identification of the MYST domain histone acetyltransferase TIP60 (HTATIP) as a co-activator of the myeloid transcription factor C/EBPα. Leukemia 22, 800–807 (2008).

Koleva, R.I. et al. C/EBPα and DEK coordinately regulate myeloid differentiation. Blood 119, 4878–4888 (2012).

Fujimoto, T., Anderson, K., Jacobsen, S.E.W., Nishikawa, S.-I. & Nerlov, C. Cdk6 blocks myeloid differentiation by interfering with Runx1 DNA binding and Runx1-C/EBPα interaction. EMBO J. 26, 2361–2370 (2007).

Wysocka, J. et al. WDR5 associates with histone H3 methylated at K4 and is essential for H3K4 methylation and vertebrate development. Cell 121, 859–872 (2005).

Bolshan, Y. et al. Synthesis, optimization, and evaluation of novel small molecules as antagonists of WDR5-MLL interaction. ACS Med. Chem. Lett. 4, 353–357 (2013).

Senisterra, G. et al. Small-molecule inhibition of MLL activity by disruption of its interaction with WDR5. Biochem. J. 449, 151–159 (2013).

Migliori, V. et al. Symmetric dimethylation of H3R2 is a newly identified histone mark that supports euchromatin maintenance. Nat. Struct. Mol. Biol. 19, 136–144 (2012).

Dias, J. et al. Structural analysis of the KANSL1/WDR5/KANSL2 complex reveals that WDR5 is required for efficient assembly and chromatin targeting of the NSL complex. Genes Dev. 28, 929–942 (2014).

Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide. Proc. Natl. Acad. Sci. USA 102, 15545–15550 (2005).

Dou, Y. et al. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat. Struct. Mol. Biol. 13, 713–719 (2006).

Couture, J.-F., Collazo, E. & Trievel, R.C. Molecular recognition of histone H3 by the WD40 protein WDR5. Nat. Struct. Mol. Biol. 13, 698–703 (2006).

Song, J.-J. & Kingston, R.E. WDR5 interacts with mixed lineage leukemia (MLL) protein via the histone H3-binding pocket. J. Biol. Chem. 283, 35258–35264 (2008).

Patel, A., Dharmarajan, V. & Cosgrove, M.S. Structure of WDR5 bound to mixed lineage leukemia protein-1 peptide. J. Biol. Chem. 283, 32158–32161 (2008).

Ruthenburg, A.J. et al. Histone H3 recognition and presentation by the WDR5 module of the MLL1 complex. Nat. Struct. Mol. Biol. 13, 704–712 (2006).

Ang, Y.-S. et al. Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 145, 183–197 (2011).

Yu, M. et al. Insights into GATA-1–mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol. Cell 36, 682–695 (2009).

Dou, Y. et al. Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 121, 873–885 (2005).

Tyagi, S., Chabes, A.L., Wysocka, J. & Herr, W. E2F activation of S phase promoters via association with HCF-1 and the MLL family of histone H3K4 methyltransferases. Mol. Cell 27, 107–119 (2007).

Cao, F. et al. Targeting MLL1 H3K4 methyltransferase activity in mixed-lineage leukemia. Mol. Cell 53, 247–261 (2014).

Lavallée-Adam, M., Cloutier, P., Coulombe, B. & Blanchette, M. Modeling contaminants in AP-MS/MS experiments. J. Proteome Res. 10, 886–895 (2011).

Zuber, J. et al. Toolkit for evaluating genes required for proliferation and survival using tetracycline-regulated RNAi. Nat. Biotechnol. 29, 79–83 (2011).

Shevchenko, A., Wilm, M., Vorm, O. & Mann, M. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68, 850–858 (1996).

Bennett, K.L. et al. Proteomic analysis of human cataract aqueous humour: Comparison of one-dimensional gel LCMS with two-dimensional LCMS of unlabelled and iTRAQ-labelled specimens. J. Proteomics 74, 151–166 (2011).

Olsen, J.V. et al. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell. Proteomics 4, 2010–2021 (2005).

Colinge, J., Masselot, A., Giron, M., Dessigny, T. & Magnin, J. OLAV: towards high-throughput tandem mass spectrometry data identification. Proteomics 3, 1454–1463 (2003).

Huber, K.V. et al. Stereospecific targeting of MTH1 by (S)-crizotinib as an anticancer strategy. Nature 508, 222–227 (2014).

Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in Os. Meth. Enzymol. 276, 307–326 (1997).

McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).

Schüttelkopf, A.W. & van Aalten, D.M.F. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. D Biol. Crystallogr. 60, 1355–1363 (2004).

Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240–255 (1997).

Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132 (2004).

Davis, I.W., Murray, L.W., Richardson, J.S. & Richardson, D.C. MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 32, W615–W619 (2004).

Siarheyeva, A. et al. An allosteric inhibitor of protein arginine methyltransferase 3. Structure 20, 1425–1435 (2012).

Yu, W. et al. Catalytic site remodelling of the DOT1L methyltransferase by selective inhibitors. Nat. Commun. 3, 1288 (2012).

Niesen, F.H., Berglund, H. & Vedadi, M. The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc. 2, 2212–2221 (2007).

Langmead, B. & Salzberg, S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).

Feng, J., Liu, T., Qin, B., Zhang, Y. & Liu, X.S. Identifying ChIP-seq enrichment using MACS. Nat. Protoc. 7, 1728–1740 (2012).

Salmon-Divon, M., Dvinge, H., Tammoja, K. & Bertone, P. PeakAnalyzer: genome-wide annotation of chromatin binding and modification loci. BMC Bioinformatics 11, 415 (2010).

Astapova, I. et al. The nuclear corepressor, NCoR, regulates thyroid hormone action in vivo. Proc. Natl. Acad. Sci. USA 105, 19544–19549 (2008).

Irizarry, R.A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249–264 (2003).

Bilban, M. et al. Deregulated expression of fat and muscle genes in B-cell chronic lymphocytic leukemia with high lipoprotein lipase expression. Leukemia 20, 1080–1088 (2006).

Schmittgen, T.D. & Livak, K.J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101–1108 (2008).