The histone lysine methyltransferase KMT2D sustains a gene expression program that represses B cell lymphoma development

Nature Medicine - Tập 21 Số 10 - Trang 1199-1208 - 2015
Ana Ortega-Molina1, Isaac W. Boss2, Andrés Canela3, Heng Pan4, Yanwen Jiang2, Chunying Zhao1, Man Jiang1, Deqing Hu5, Xabier Agirre2, Itamar Niesvizky6, Ji‐Eun Lee7, Hua-Tang Chen3, Daisuke Ennishi8, David W. Scott8, Anja Mottok8, Christoffer Hother8, Shichong Liu9, Xing-Jun Cao9, Wayne Tam10, Rita Shaknovich2, Benjamin A. García9, Randy D. Gascoyne8, Kai Ge7, Ali Shilatifard5, Olivier Elemento4, André Nussenzweig3, Ari Melnick6, Hans‐Guido Wendel1
1Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center (MSKCC), New York, New York, USA
2Division of Hematology-Oncology, Department of Medicine, Weill Cornell Medical College, New York, New York, USA
3Laboratory of Genome Integrity, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, USA
4Institute for Computational Biomedicine, Weill Cornell Medical College, New York, New York, USA
5Department of Biochemistry and Molecular Genetics, Northwestern University, Chicago, Illinois, USA
6Department of Pharmacology, Weill Cornell Medical College, New York, New York, USA
7Laboratory of Endocrinology and Receptor Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland, USA
8Centre for Lymphoid Cancer, British Columbia Cancer Agency. Vancouver, British Columbia, Canada
9Department of Biochemistry and Biophysics, Epigenetics Program, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
10Department of Pathology and Laboratory Medicine, Weill Cornell Medical College, New York, New York, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

De Silva, N.S. & Klein, U. Dynamics of B cells in germinal centres. Nat. Rev. Immunol. 15, 137–148 (2015).

Kridel, R., Sehn, L.H. & Gascoyne, R.D. Pathogenesis of follicular lymphoma. J. Clin. Invest. 122, 3424–3431 (2012).

Morin, R.D. et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature 476, 298–303 (2011).

Pasqualucci, L. et al. Inactivating mutations of acetyltransferase genes in B cell lymphoma. Nature 471, 189–195 (2011).

Hu, D. et al. The MLL3-MLL4 branches of the COMPASS family function as major histone H3K4 monomethylases at enhancers. Mol. Cell. Biol. 33, 4745–4754 (2013).

Herz, H.M. et al. Enhancer-associated H3K4 monomethylation by Trithorax-related, the Drosophila homolog of mammalian Mll3/Mll4. Genes Dev. 26, 2604–2620 (2012).

Lee, J.E. et al. H3K4 mono- and dimethyltransferase MLL4 is required for enhancer activation during cell differentiation. eLife 2, e01503 (2013).

Herz, H.M., Hu, D. & Shilatifard, A. Enhancer malfunction in cancer. Mol. Cell 53, 859–866 (2014).

Egle, A. VavP-Bcl2 transgenic mice develop follicular lymphoma preceded by germinal center hyperplasia. Blood 103, 2276–2283 (2004).

Oricchio, E. et al. The Eph-receptor A7 is a soluble tumor suppressor for follicular lymphoma. Cell 147, 554–564 (2011).

Stadtfeld, M. & Graf, T. Assessing the role of hematopoietic plasticity for endothelial and hepatocyte development by noninvasive lineage tracing. Development 132, 203–213 (2005).

Santos, M.A. et al. DNA damage–induced differentiation of leukemic cells as an anti-cancer barrier. Nature 514, 107–111 (2014).

Hoffman, J.D. et al. Immune abnormalities are a frequent manifestation of Kabuki syndrome. Am. J. Med. Genet. A. 135, 278–281 (2005).

Compagno, M. et al. Mutations of multiple genes cause deregulation of NF-κB in diffuse large B cell lymphoma. Nature 459, 717–721 (2009).

Molavi, O. et al. Gene methylation and silencing of SOCS3 in mantle cell lymphoma. Br. J. Haematol. 161, 348–356 (2013).

Cheung, K.J. et al. Acquired TNFRSF14 mutations in follicular lymphoma are associated with worse prognosis. Cancer Res. 70, 9166–9174 (2010).

Guo, C. et al. KMT2D maintains neoplastic cell proliferation and global histone H3 lysine 4 monomethylation. Oncotarget 4, 2144–2153 (2013).

Sarma, V. et al. Activation of the B cell surface receptor CD40 induces A20, a novel zinc-finger protein that inhibits apoptosis. J. Biol. Chem. 270, 12343–12346 (1995).

Hsing, Y., Hostager, B.S. & Bishop, G.A. Characterization of CD40 signaling determinants regulating nuclear factor-kappa B activation in B lymphocytes. J. Immunol. 159, 4898–4906 (1997).

Hollmann, C.A., Owens, T., Nalbantoglu, J., Hudson, T.J. & Sladek, R. Constitutive activation of extracellular signal–regulated kinase predisposes diffuse large B cell lymphoma cell lines to CD40-mediated cell death. Cancer Res. 66, 3550–3557 (2006).

Bjornsson, H.T. et al. Histone deacetylase inhibition rescues structural and functional brain deficits in a mouse model of Kabuki syndrome. Sci. Transl. Med. 6, 256ra135 (2014).

Højfeldt, J.W., Agger, K. & Helin, K. Histone lysine demethylases as targets for anticancer therapy. Nat. Rev. Drug Discov. 12, 917–930 (2013).

Li, H. & Durbin, R. Fast and accurate short-read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

Jiang, Y., Soong, T.D., Wang, L., Melnick, A.M. & Elemento, O. Genome-wide detection of genes targeted by non-Ig somatic hypermutation in lymphoma. PLoS ONE 7, e40332 (2012).

Wacker, S.A., Houghtaling, B.R., Elemento, O. & Kapoor, T.M. Using transcriptome sequencing to identify mechanisms of drug action and resistance. Nat. Chem. Biol. 8, 235–237 (2012).

Rajadhyaksha, A.M. et al. Mutations in FLVCR1 cause posterior column ataxia and retinitis pigmentosa. Am. J. Hum. Genet. 87, 643–654 (2010).

Scott, D.W. et al. Determining cell-of-origin subtypes of diffuse large B cell lymphoma using gene expression in formalin-fixed paraffin-embedded tissue. Blood 123, 1214–1217 (2014).

Hans, C.P. et al. Confirmation of the molecular classification of diffuse large B cell lymphoma by immunohistochemistry using a tissue microarray. Blood 103, 275–282 (2004).

Wendel, H.G. et al. Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 428, 332–337 (2004).

Dickins, R.A. et al. Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat. Genet. 37, 1289–1295 (2005).

Béguelin, W. et al. EZH2 is required for germinal center formation and somatic EZH2 mutations promote lymphoid transformation. Cancer Cell 23, 677–692 (2013).

Mavrakis, K.J. et al. Tumorigenic activity and therapeutic inhibition of Rheb GTPase. Genes Dev. 22, 2178–2188 (2008).

Hanna, J. et al. Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell 133, 250–264 (2008).

Ehlich, A., Martin, V., Muller, W. & Rajewsky, K. Analysis of the B cell progenitor compartment at the level of single cells. Curr. Biol. 4, 573–583 (1994).

Gostissa, M. et al. Conditional inactivation of p53 in mature B cells promotes generation of nongerminal center–derived B cell lymphomas. Proc. Natl. Acad. Sci. USA 110, 2934–2939 (2013).

Brochet, X., Lefranc, M.P. & Giudicelli, V. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 36, W503–W508 (2008).

Robbiani, D.F. et al. AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell 135, 1028–1038 (2008).

Ci, W. et al. The BCL6 transcriptional program features repression of multiple oncogenes in primary B cells and is deregulated in DLBCL. Blood 113, 5536–5548 (2009).

Lee, T.I., Johnstone, S.E. & Young, R.A. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 1, 729–748 (2006).

Goodarzi, H., Elemento, O. & Tavazoie, S. Revealing global regulatory perturbations across human cancers. Mol. Cell 36, 900–911 (2009).

Cover, T.M. & Thomas, J.A. Elements of Information Theory (Wiley-Interscience, Hoboken, N.J., 2006).

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

Shaffer, A.L. et al. A library of gene expression signatures to illuminate normal and pathological lymphoid biology. Immunol. Rev. 210, 67–85 (2006).

Mootha, V.K. et al. PGC-1α–responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267–273 (2003).

Mavrakis, K.J. & Wendel, H.G. Translational control and cancer therapy. Cell Cycle 7, 2791–2794 (2008).

Lin, S. & Garcia, B.A. Examining histone posttranslational modification patterns by high-resolution mass spectrometry. Methods Enzymol. 512, 3–28 (2012).

Yuan, Z.F. et al. EpiProfile quantifies histone peptides with modifications by extracting retention time and intensity in high-resolution mass spectra. Mol. Cell. Proteomics 14, 1696–1707 (2015).

Festing, M.F.W. & Laboratory Animals Ltd. The Design of Animal Experiments: Reducing the Use of Animals in Research Through Better Experimental Design (Royal Society of Medicine, London, 2002).