Disruption of KMT2D perturbs germinal center B cell development and promotes lymphomagenesis

Nature Medicine - Tập 21 Số 10 - Trang 1190-1198 - 2015
Jiyuan Zhang1, David Dominguez-Sola1, Shafinaz Hussein1, Ji‐Eun Lee2, Antony B. Holmes1, Mukesh Bansal3, Sofija Vlasevska1, Tongwei Mo1, Hongyan Tang1, Katia Basso1, Kai Ge2, Riccardo Dalla‐Favera1, Laura Pasqualucci4
1Institute for Cancer Genetics, Columbia University, New York, New York, USA
2Laboratory of Endocrinology and Receptor Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland, USA
3Department of Systems Biology, Columbia University, New York, New York, USA
4Department of Pathology and Cell Biology, Columbia University, New York, New York, USA

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Shaffer III, A.L., Young, R.M. & Staudt, L.M. Pathogenesis of human B cell lymphomas. Annu. Rev. Immunol. 30, 565–610 (2012).

Basso, K. & Dalla-Favera, R. Germinal centers and B cell lymphomagenesis. Nat. Rev. Immunol. 15, 172–184 (2015).

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).

Pasqualucci, L. et al. Analysis of the coding genome of diffuse large B cell lymphoma. Nat. Genet. 43, 830–837 (2011).

Lohr, J.G. et al. Discovery and prioritization of somatic mutations in diffuse large B cell lymphoma (DLBCL) by whole-exome sequencing. Proc. Natl. Acad. Sci. USA 109, 3879–3884 (2012).

Okosun, J. et al. Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat. Genet. 46, 176–181 (2014).

Pasqualucci, L. et al. Genetics of follicular lymphoma transformation. Cell Rep. 6, 130–140 (2014).

Alizadeh, A.A. et al. Distinct types of diffuse large B cell lymphoma identified by gene expression profiling. Nature 403, 503–511 (2000).

Green, M.R. et al. Hierarchy in somatic mutations arising during genomic evolution and progression of follicular lymphoma. Blood 121, 1604–1611 (2013).

Green, M.R. et al. Mutations in early follicular lymphoma progenitors are associated with suppressed antigen presentation. Proc. Natl. Acad. Sci. USA 112, E1116–E1125 (2015).

Shilatifard, A. The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu. Rev. Biochem. 81, 65–95 (2012).

Kouzarides, T. Chromatin modifications and their function. Cell 128, 693–705 (2007).

Li, B., Carey, M. & Workman, J.L. The role of chromatin during transcription. Cell 128, 707–719 (2007).

Briggs, S.D. et al. Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 15, 3286–3295 (2001).

Roguev, A. et al. The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J. 20, 7137–7148 (2001).

Miller, T. et al. COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc. Natl. Acad. Sci. USA 98, 12902–12907 (2001).

Krogan, N.J. et al. COMPASS, a histone H3 (lysine 4) methyltransferase required for telomeric silencing of gene expression. J. Biol. Chem. 277, 10753–10755 (2002).

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).

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).

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

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

Kaikkonen, M.U. et al. Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription. Mol. Cell 51, 310–325 (2013).

Ng, S.B. et al. Exome sequencing identifies MLL2 mutations as a cause of Kabuki syndrome. Nat. Genet. 42, 790–793 (2010).

Guo, C. et al. Global identification of MLL2-targeted loci reveals MLL2's role in diverse signaling pathways. Proc. Natl. Acad. Sci. USA 109, 17603–17608 (2012).

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

Dhar, S.S. et al. Trans-tail regulation of MLL4-catalyzed H3K4 methylation by H4R3 symmetric dimethylation is mediated by a tandem PHD of MLL4. Genes Dev. 26, 2749–2762 (2012).

Casola, S. et al. Tracking germinal center B cells expressing germline immunoglobulin γ1 transcripts by conditional gene targeting. Proc. Natl. Acad. Sci. USA 103, 7396–7401 (2006).

Rickert, R.C., Roes, J. & Rajewsky, K. B lymphocyte–specific, Cre-mediated mutagenesis in mice. Nucleic Acids Res. 25, 1317–1318 (1997).

Carsetti, R., Kohler, G. & Lamers, M.C. Transitional B cells are the target of negative selection in the B cell compartment. J. Exp. Med. 181, 2129–2140 (1995).

Allman, D. et al. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167, 6834–6840 (2001).

Jacob, J. & Kelsoe, G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. II. A common clonal origin for periarteriolar lymphoid sheath–associated foci and germinal centers. J. Exp. Med. 176, 679–687 (1992).

Lim, W.K., Lyashenko, E. & Califano, A. Master regulators used as breast cancer metastasis classifier. Pacific Symposium on Biocomputing 504–515 (2009).

Pao, L.I. et al. B cell–specific deletion of protein-tyrosine phosphatase Shp1 promotes B-1a cell development and causes systemic autoimmunity. Immunity 27, 35–48 (2007).

Yokouchi, M., Suzuki, R., Masuhara, M., Komiya, S., Inoue, A. & Yoshimura, A. Cloning and characterization of APS, an adaptor molecule containing PH and SH2 domains that is tyrosine phosphorylated upon B cell receptor stimulation. Oncogene 15, 7–15 (1997).

Sauer, K. & Cooke, M.P. Regulation of immune cell development through soluble inositol-1,3,4,5-tetrakisphosphate. Nat. Rev. Immunol. 10, 257–271 (2010).

Liu, Y.J. et al. Mechanism of antigen-driven selection in germinal centers. Nature 342, 929–931 (1989).

Egle, A., Harris, A.W., Bath, M.L., O'Reilly, L. & Cory, S. VavP-Bcl2 transgenic mice develop follicular lymphoma preceded by germinal center hyperplasia. Blood 103, 2276–2283 (2004).

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

Zhang, J. et al. Genetic heterogeneity of diffuse large B cell lymphoma. Proc. Natl. Acad. Sci. USA 110, 1398–1403 (2013).

Creyghton, M.P. et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. USA 107, 21931–21936 (2010).

Rada-Iglesias, A. et al. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470, 279–283 (2011).

Whyte, W.A. et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153, 307–319 (2013).

Chapuy, B. et al. Discovery and characterization of super-enhancer–associated dependencies in diffuse large B cell lymphoma. Cancer Cell 24, 777–790 (2013).

Ardehali, M.B. et al. Drosophila Set1 is the major histone H3 lysine 4 trimethyltransferase with role in transcription. EMBO J. 30, 2817–2828 (2011).

Calo, E. & Wysocka, J. Modification of enhancer chromatin: what, how and why? Mol. Cell 49, 825–837 (2013).

Petruk, S. et al. TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell 150, 922–933 (2012).

Pasqualucci, L. The genetic basis of diffuse large B cell lymphoma. Curr. Opin. Hematol. 20, 336–344 (2013).

Pasqualucci, L. et al. AID is required for germinal center–derived lymphomagenesis. Nat. Genet. 40, 108–112 (2008).

Pasqualucci, L. et al. Hypermutation of multiple proto-oncogenes in B cell diffuse large-cell lymphomas. Nature 412, 341–346 (2001).

Hatzi, K. & Melnick, A. Breaking bad in the germinal center: how deregulation of BCL6 contributes to lymphomagenesis. Trends Mol. Med. 20, 343–352 (2014).

Cattoretti, G. et al. Deregulated BCL6 expression recapitulates the pathogenesis of human diffuse large B cell lymphomas in mice. Cancer Cell 7, 445–455 (2005).

Mandelbaum, J. et al. BLIMP1 is a tumor suppressor gene frequently disrupted in activated B cell–like diffuse large B cell lymphoma. Cancer Cell 18, 568–579 (2010).

Souers, A.J. et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat. Med. 19, 202–208 (2013).

Knutson, S.K. et al. A selective inhibitor of EZH2 blocks H3K27 methylation and kills mutant lymphoma cells. Nat. Chem. Biol. 8, 890–896 (2012).

McCabe, M.T. et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature 492, 108–112 (2012).

Klein, U. et al. Transcriptional analysis of the B cell germinal center reaction. Proc. Natl. Acad. Sci. USA 100, 2639–2644 (2003).

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

Dominguez-Sola, D. et al. The proto-oncogene is required for selection in the germinal center and cyclic reentry. Nat. Immunol. 13, 1083–1091 (2012).

Thomas, M. et al. Full deacylation of polyethylenimine dramatically boosts its gene delivery efficiency and specificity to mouse lung. Proc. Natl. Acad. Sci. USA 102, 5679–5684 (2005).

Bereshchenko, O.R., Gu, W. & Dalla-Favera, R. Acetylation inactivates the transcriptional repressor BCL6. Nat. Genet. 32, 606–613 (2002).

Livak, K.J. & Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408 (2001).

Green, M.R. & Sambrook, J. Molecular Cloning: A Laboratory Manual 4th edn. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA, 2012).

Jolly, C.J., Klix, N. & Neuberger, M.S. Rapid methods for the analysis of immunoglobulin gene hypermutation: application to transgenic and gene-targeted mice. Nucleic Acids Res. 25, 1913–1919 (1997).

Klein, U. et al. Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat. Immunol. 7, 773–782 (2006).

Reich, M. et al. GenePattern 2.0. Nat. Genet. 38, 500–501 (2006).

Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate–a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289–300 (1995).

Subramanian, A., Kuehn, H., Gould, J., Tamayo, P. & Mesirov, J.P. GSEA-P: a desktop application for gene set enrichment analysis. Bioinformatics 23, 3251–3253 (2007).

Huang, D.W., Sherman, B.T. & Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44–57 (2009).

Blecher-Gonen, R. et al. High-throughput chromatin immunoprecipitation for genome-wide mapping of in vivo protein-DNA interactions and epigenomic states. Nat. Protoc. 8, 539–554 (2013).

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

Li, H. et al. The sequence alignment–map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

Giannopoulou, E.G. & Elemento, O. An integrated ChIP-seq analysis platform with customizable workflows. BMC Bioinformatics 12, 277 (2011).

Lin, C.Y. et al. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151, 56–67 (2012).

Lovén, J. et al. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 153, 320–334 (2013).