EZH2 and BCL6 Cooperate to Assemble CBX8-BCOR Complex to Repress Bivalent Promoters, Mediate Germinal Center Formation and Lymphomagenesis
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The EZH2 histone methyltransferase mediates the humoral immune response and drives lymphomagenesis through formation of bivalent chromatin domains at critical germinal center (GC) B cell promoters. Herein we show that the actions of EZH2 in driving GC formation and lymphoma precursor lesions require site-specific binding by the BCL6 transcriptional repressor and the presence of a non-canonical PRC1-BCOR-CBX8 complex. The chromodomain protein CBX8 is induced in GC B cells, binds to H3K27me3 at bivalent promoters, and is required for stable association of the complex and the resulting histone modifications. Moreover, oncogenic BCL6 and EZH2 cooperate to accelerate diffuse large B cell lymphoma (DLBCL) development and combinatorial targeting of these repressors results in enhanced anti-lymphoma activity in DLBCLs.
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In yeast, Dot1 promotes DNA repair via homologous recombination.
“In yeast, Dot1 promotes DNA repair via homologous recombination”
From The roles of DNA, RNA and histone methylation in ageing and cancer (2019) · cites this paper as [204]
In mammalian cells, DOT1L depletion leads to defects in DNA repair, enhancing sensitivity to DNA damaging agents.
“in mammalian cells DOT1L depletion leads to defects in DNA repair, enhancing sensitivity to DNA damaging agents 203,204”
From The roles of DNA, RNA and histone methylation in ageing and cancer (2019) · cites this paper as [204]
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Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · see citing works
A bivalent chromatin structure marks key developmental genes in embryonic stem cells
Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., et al. (2006) · Cell · doi:10.1016/j.cell.2006.02.041 · Cited by 5,361 · see citing works
EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations
McCabe, M. T., Ott, H. M., Ganji, G., Korenchuk, S., Thompson, C., Van Aller, G. S., Liu, Y., Graves, A. P., III, A. D. P., Diaz, E., et al. (2012) · Nature · doi:10.1038/nature11606 · Cited by 1,786 · see citing works
Morin, R. D., Johnson, N. A., Severson, T., Mungall, A. J. J., An, J., Goya, R., Paul, J. E., Boyle, M., Woolcock, B. W., Kuchenbauer, F. C., et al. (2010) · Nature Genetics · doi:10.1038/ng.518 · Cited by 1,670 · see citing works
Self-citationMechanisms of Polycomb gene silencing: knowns and unknowns
Simon, J. A., & Kingston, R. E. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2763 · Cited by 1,320 · see citing works
Béguelin, W., Popovic, R., Teater, M. R., Jiang, Y., Bunting, K. L., Rosen, M., Shen, H., Yang, S. N., Wang, L., Ezponda, T., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.04.011 · Cited by 854 · see citing works
Self-citationPCGF Homologs, CBX Proteins, and RYBP Define Functionally Distinct PRC1 Family Complexes
Gao, Z., Zhang, J., Bonasio, R., Strino, F., Sawai, A., Parisi, F., Kluger, Y., & Reinberg, D. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.01.002 · Cited by 852 · see citing works
A selective inhibitor of EZH2 blocks H3K27 methylation and kills mutant lymphoma cells
Knutson, S. K., Wigle, T. J., Warholic, N. M., Sneeringer, C. J., Allain, C. J., Klaus, C. R., Sacks, J. D., Raimondi, A., Majer, C. R., Song, J., et al. (2012) · Nature Chemical Biology · doi:10.1038/nchembio.1084 · Cited by 776 · see citing works
Blackledge, N. P., Farcas, A. M., Kondo, T., King, H. W., McGouran, J. F., Hanssen, L. L. P., Ito, S., Cooper, S., Kondo, K., Koseki, Y., et al. (2014) · Cell · doi:10.1016/j.cell.2014.05.004 · Cited by 734 · see citing works
Sequence and structural analysis of BTB domain proteins
Stogios, P. J., Downs, G. S., Jauhal, J. J., Nandra, S. K., & Privé, G. G. (2005) · Genome Biology · doi:10.1186/gb-2005-6-10-r82 · Cited by 694 · see citing works
Sneeringer, C. J., Scott, M. P., Kuntz, K. W., Knutson, S. K., Pollock, R. M., Richon, V. M., & Copeland, R. A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012525107 · Cited by 691 · see citing works
Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement
Su, I.-H., Basavaraj, A., Krutchinsky, A. N., Hobert, O., Ullrich, A., Chait, B. T., & Tarakhovsky, A. (2002) · Nature Immunology · doi:10.1038/ni876 · Cited by 614 · see citing works
H3K36 Methylation Antagonizes PRC2-mediated H3K27 Methylation
Yuan, W., Xu, M., Huang, C., Liu, N., Chen, S., & Zhu, B. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.194027 · Cited by 537 · see citing works
BCoR, a novel corepressor involved in BCL-6 repressionPreprint
Huynh, K. D., Fischle, W., Verdin, E. M., & Bardwell, V. J. (2000) · Genes & Development · doi:10.1101/gad.14.14.1810 · Cited by 475 · see citing works
Self-citationKDM2B links the Polycomb Repressive Complex 1 (PRC1) to recognition of CpG islands
Farcas, A. M., Blackledge, N. P., Sudbery, I. M., Long, H. K., McGouran, J. F., Rose, N. R., Lee, S., Sims, D., Cerase, A., Sheahan, T. W., et al. (2012) · eLife · doi:10.7554/elife.00205 · Cited by 472 · see citing works
Histone H2A monoubiquitination promotes histone H3 methylation in Polycomb repression
Kalb, R., Latwiel, S., Baymaz, H. I., Jansen, P. W. T. C., Müller, C. W., Vermeulen, M., & Müller, J. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2833 · Cited by 451 · see citing works
Recruitment of Polycomb group complexes and their role in the dynamic regulation of cell fate choice
Schuettengruber, B., & Cavalli, G. (2009) · Development · doi:10.1242/dev.033902 · Cited by 424 · see citing works
Cattoretti, G., Pasqualucci, L., Ballon, G., Tam, W., Nandula, S. V., Shen, Q., Mo, T., Murty, V. V., & Dalla-Favera, R. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.03.037 · Cited by 383 · see citing works
Fbxl10/Kdm2b Recruits Polycomb Repressive Complex 1 to CpG Islands and Regulates H2A Ubiquitylation
Wu, X., Johansen, J. V., & Helin, K. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.016 · Cited by 375 · see citing works
Gearhart, M. D., Corcoran, C. M., Wamstad, J. A., & Bardwell, V. J. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00630-06 · Cited by 352 · see citing works
Self-citationEZH2 mutations are frequent and represent an early event in follicular lymphoma
Bödör, C., Großmann, V., Popov, N., Okosun, J., Ó’Riain, C., Tan, K. L., Marzec, J., Araf, S., Wang, J., Lee, A. M., et al. (2013) · Blood · doi:10.1182/blood-2013-04-496893 · Cited by 325 · see citing works
Self-citationCooper, S., Dienstbier, M., Hassan, R., Schermelleh, L., Sharif, J., Blackledge, N. P., Marco, V. D., Elderkin, S., Koseki, H., Klose, R. J., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.04.012 · Cited by 323 · see citing works
Recognition and Specificity Determinants of the Human Cbx Chromodomains
Kaustov, L., Ouyang, H., Amaya, M. F., Lemak, A. S., Nady, N., Duan, S., Wasney, G. A., Li, Z., Vedadi, M., Schapira, M., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.191411 · Cited by 306 · see citing works
Velichutina, I., Shaknovich, R., Geng, H., Johnson, N. A., Gascoyne, R. D., Melnick, A. M., & Elemento, O. (2010) · Blood · doi:10.1182/blood-2010-04-280149 · Cited by 299 · see citing works
Self-citationA Small-Molecule Inhibitor of BCL6 Kills DLBCL Cells In Vitro and In Vivo
Cerchietti, L. C., Ghetu, A. F., Zhu, X., Da Silva, G. F., Zhong, S., Matthews, M., Bunting, K. L., Polo, J. M., Farès, C., Arrowsmith, C. H., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2009.12.050 · Cited by 288 · see citing works
Self-citationYe, B. H., Chaganti, S., Chang, C., Niu, H., Corradini, P., Chaganti, R. S. K., & Dalla‐Favera, R. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb00311.x · Cited by 278 · see citing works
Germinal center dysregulation by histone methyltransferase EZH2 promotes lymphomagenesis
Cagánová, M., Carrisi, C., Varano, G., Mainoldi, F., Zanardi, F., Germain, P., George, L. A., Alberghini, F., Ferrarini, L., Talukder, A. K., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci70626 · Cited by 256 · see citing works
Casola, S. S., Cattoretti, G., Uyttersprot, N., Koralov, S. B., Seagal, J., Hao, Z., Waisman, A., Egert, A., Ghitza, D., & Rajewsky, K. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602353103 · Cited by 239 · see citing works
Sánchez, C., Sánchez, I., Demmers, J., Rodriguez, P., Strouboulis, J., & Vidal, M. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600275-mcp200 · Cited by 223 · see citing works
Hatzi, K., Jiang, Y., Huang, C., Garrett-Bakelman, F. E., Gearhart, M. D., Γιαννοπούλου, Ε., Zumbo, P., Kirouac, K. N., Bhaskara, S., Polo, J. M., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.06.016 · Cited by 186 · see citing works
Self-citationBreaking bad in the germinal center: how deregulation of BCL6 contributes to lymphomagenesis
Hatzi, K., & Melnick, A. (2014) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.03.001 · Cited by 183 · see citing works
Self-citationRationally designed BCL6 inhibitors target activated B cell diffuse large B cell lymphoma
Cardenas, M. G., Yu, W., Beguelin, W., Teater, M. R., Geng, H., Goldstein, R. L., Oswald, E., Hatzi, K., Yang, S.-N., Cohen, J., et al. (2016) · Journal of Clinical Investigation · doi:10.1172/jci85795 · Cited by 176 · see citing works
Self-citationCBX8, a Polycomb Group Protein, Is Essential for MLL-AF9-Induced Leukemogenesis
Tan, J., Jones, M., Koseki, H., Nakayama, M., Muntean, A. G., Maillard, I. P., & Hess, J. L. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.09.008 · Cited by 172 · see citing works
Structure of a BCOR Corepressor Peptide in Complex with the BCL6 BTB Domain Dimer
Ghetu, A. F., Corcoran, C. M., Cerchietti, L., Bardwell, V. J., Melnick, A., & Privé, G. G. (2008) · Molecular Cell · doi:10.1016/j.molcel.2007.12.026 · Cited by 168 · see citing works
Self-citationVandamme, J., Völkel, P., Rosnoblet, C., Faou, P. L., & Angrand, P. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.002642 · Cited by 143 · see citing works
Huang, C., Hatzi, K., & Melnick, A. M. (2013) · Nature Immunology · doi:10.1038/ni.2543 · Cited by 139 · see citing works
Self-citationChromatin Sampling—An Emerging Perspective on Targeting Polycomb Repressor Proteins
Klose, R. J., Cooper, S., Farcas, A. M., Blackledge, N. P., & Brockdorff, N. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003717 · Cited by 129 · see citing works
Junco, S. E., Wang, R., Gaipa, J. C., Taylor, A. B., Schirf, V. R., Gearhart, M. D., Bardwell, V. J., Demeler, B., Hart, P. J., & Kim, C. A. (2013) · Structure · doi:10.1016/j.str.2013.02.013 · Cited by 120 · see citing works
Self-citationPolycomb Group Targeting through Different Binding Partners of RING1B C-Terminal Domain
Wang, R., Taylor, A. B., Leal, B. Z., Chadwell, L. V., Ilangovan, U., Robinson, A. K., Schirf, V. R., Hart, P. J., Lafer, E. M., Demeler, B., et al. (2010) · Structure · doi:10.1016/j.str.2010.04.013 · Cited by 100 · see citing works
Raaphorst, F. M., van Kemenade, F. J., Fieret, E. J. H., Hamer, K. M., Satijn, D. P. E., Otte, A. P., & Meijer, C. J. L. M. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.1.1 · Cited by 98 · see citing works
B-cell lymphoma 6 and the molecular pathogenesis of diffuse large B-cell lymphoma
Ci, W., Polo, J. M., & Melnick, A. M. (2008) · Current Opinion in Hematology · doi:10.1097/moh.0b013e328302c7df · Cited by 86 · see citing works
Self-citationCreppe, C., Palau, A., Malinverni, R., Valero, V., & Buschbeck, M. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004851 · Cited by 68 · see citing works
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Crotty, S. (2019) · Immunity · doi:10.1016/j.immuni.2019.04.011 · Cited by 1,591 · see citing works
Morschhauser, F., Tilly, H., Chaidos, A., McKay, P., Phillips, T., Assouline, S. E., Batlevi, C. L., Campbell, P., Ribrag, V., Damaj, G. L., et al. (2020) · The Lancet Oncology · doi:10.1016/s1470-2045(20)30441-1 · Cited by 612 · see citing works
The roles of DNA, RNA and histone methylation in ageing and cancer
Michalak, E. M., Burr, M. L., Bannister, A. J., & Dawson, M. A. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0143-1 · Cited by 549 · see citing works
The molecular principles of gene regulation by Polycomb repressive complexes
Blackledge, N. P., & Klose, R. J. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00398-y · Cited by 470 · see citing works
Ennishi, D., Takata, K., Béguelin, W., Duns, G., Mottok, A., Farinha, P., Bashashati, A., Saberi, S., Boyle, M., Meissner, B., et al. (2019) · Cancer Discovery · doi:10.1158/2159-8290.cd-18-1090 · Cited by 318 · see citing works
“Conditional Ezh2Y641F knock-in and transgenic Ezh2Y641N mice were generated as described previously (27, 34).”
MethodSelf-citationEffect of ibrutinib with R-CHOP chemotherapy in genetic subtypes of DLBCL
Wilson, W. H., Wright, G. W., Huang, D. W., Hodkinson, B. P., Balasubramanian, S., Fan, Y., VERMEULEN, J. T., Shreeve, S. M., & Staudt, L. M. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.10.006 · Cited by 320 · see citing works
Germinal centers: programmed for affinity maturation and antibody diversification
Bannard, O., & Cyster, J. G. (2017) · Current Opinion in Immunology · doi:10.1016/j.coi.2016.12.004 · Cited by 199 · see citing works
Enhancer of zeste homolog 2 (EZH2) inhibitors
Gulati, N., Béguelin, W., & Giulino-Roth, L. G. (2018) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428194.2018.1430795 · Cited by 196 · see citing works
Self-citationDangerous liaisons: interplay between SWI/SNF, NuRD, and Polycomb in chromatin regulation and cancerPreprint
Bracken, A. P., Brien, G. L., & Verrijzer, C. P. (2019) · Genes & Development · doi:10.1101/gad.326066.119 · Cited by 192 · see citing works
Astolfi, A., Fiore, M., Melchionda, F., Indio, V., Bertuccio, S. N., & Pession, A. (2019) · Epigenomics · doi:10.2217/epi-2018-0195 · Cited by 183 · see citing works
Béguelin, W., Rivas, M. A., Calvo, M. T., Teater, M. R., Purwada, A., Redmond, D., Shen, H., Challman, M. F., Elemento, O., Singh, A., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01029-x · Cited by 183 · see citing works
Self-citationCurrent State of Knowledge on Primary Sjögren’s Syndrome, an Autoimmune Exocrinopathy
Parisis, D., Chivasso, C., Perret, J., Soyfoo, M. S., & Delporte, C. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9072299 · Cited by 183 · see citing works
The Expanding Role of the BCL6 Oncoprotein as a Cancer Therapeutic Target
Cárdenas, M., Oswald, E. M., Yu, W., Xue, F., MacKerell, A. D., & Melnick, A. M. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-2071 · Cited by 181 · see citing works
Self-citationGerminal center‐derived lymphomas: The darkest side of humoral immunity
Mlynarczyk, C., Fontán, L., & Melnick, A. (2019) · Immunological Reviews · doi:10.1111/imr.12755 · Cited by 179 · see citing works
Self-citationExtracellular vesicle-mediated delivery of miR-101 inhibits lung metastasis in osteosarcoma
Zhang, K., Dong, C., Chen, M., Yang, T.-T., Wang, X., Gao, Y., Wang, L., Wen, Y., Chen, G., Wang, X., et al. (2019) · Theranostics · doi:10.7150/thno.33482 · Cited by 172 · see citing works
Mondello, P., Tadros, S., Teater, M., Fontan, L., Chang, A. Y., Jain, N., Yang, H., Singh, S., Ying, H.-Y., Chu, C.-S., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-0116 · Cited by 167 · see citing works
Self-citationMutant EZH2 Induces a Pre-malignant Lymphoma Niche by Reprogramming the Immune Response
Béguelin, W., Teater, M. R., Meydan, C., Hoehn, K. B., Phillip, J. M., Soshnev, A. A., Venturutti, L., Rivas, M. A., Calvo, M. T., Gutierrez, J., et al. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.04.004 · Cited by 161 · see citing works
Self-citationMechanisms of Polycomb group protein function in cancer
Parreno, V., Martinez, A., & Cavalli, G. (2022) · Cell Research · doi:10.1038/s41422-021-00606-6 · Cited by 147 · see citing works
Chromatin modifying gene mutations in follicular lymphoma
Green, M. R. (2017) · Blood · doi:10.1182/blood-2017-08-737361 · Cited by 141 · see citing works
Zhang, Y., Kang, M., Zhang, B., Meng, F., Song, J. H., Kaneko, H., Shimamoto, F., & Tang, B. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1116-x · Cited by 140 · see citing works
RetractedGuo, M., Price, M. J., Patterson, D. G., Barwick, B. G., Haines, R. R., Kania, A. K., Bradley, J., Randall, T. D., Boss, J. M., & Scharer, C. D. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1701470 · Cited by 136 · see citing works
From genetics to the clinic: a translational perspective on follicular lymphoma
Huet, S., Sujobert, P., & Salles, G. (2018) · Nature reviews. Cancer · doi:10.1038/nrc.2017.127 · Cited by 135 · see citing works
Uenishi, G. I., Jung, H. S., Kumar, A., Park, M. A., Hadland, B., McLeod, E., Raymond, M., Moskvin, O. V., Zimmerman, C., Theisen, D. J., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04134-7 · Cited by 134 · see citing works
Plasma cell differentiation is controlled by multiple cell division-coupled epigenetic programs
Scharer, C. D., Barwick, B. G., Guo, M., Bally, A. P. R., & Boss, J. M. (2018) · Nature Communications · doi:10.1038/s41467-018-04125-8 · Cited by 130 · see citing works
Emerging epigenetic-modulating therapies in lymphoma
Sermer, D. J., Pasqualucci, L., Wendel, H., Melnick, A. M., & Younes, A. (2019) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-019-0190-8 · Cited by 120 · see citing works
Self-citationEZH2 function in immune cell development
Nutt, S. L., Keenan, C. R., Chopin, M., & Allan, R. S. (2020) · Biological Chemistry · doi:10.1515/hsz-2019-0436 · Cited by 110 · see citing works
Genetic and epigenetic determinants of diffuse large B-cell lymphoma
Bakhshi, T. J., & Georgel, P. T. (2020) · Blood Cancer Journal · doi:10.1038/s41408-020-00389-w · Cited by 107 · see citing works
A Non-canonical BCOR-PRC1.1 Complex Represses Differentiation Programs in Human ESCs
Wang, Z., Gearhart, M. D., Lee, Y.-W., Kumar, I., Ramazanov, B. R., Zhang, Y., Hernandez, C. C., Lü, A., Neuenkirchen, N., Deng, J., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2017.12.002 · Cited by 104 · see citing works
Self-citationLiu, Y., Peng, J., Sun, T., Li, N., Zhang, L., Ren, J., Yuan, H., Kan, S., Pan‐Hammarström, Q., Li, X., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1700909114 · Cited by 102 · see citing works
Jiang, Q., Isquith, J. M., Zipeto, M., Diep, R. H., Pham, J., Santos, N. P. D., Reynoso, E., Chau, J., Leu, H. S., Lazzari, E., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2018.11.017 · Cited by 100 · see citing works
Toward a New Molecular Taxonomy of Diffuse Large B-cell Lymphoma
Ennishi, D., Hsi, E. D., Steidl, C., & Scott, D. W. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-0174 · Cited by 96 · see citing works
Agirre, X., Meydan, C., Jiang, Y., Gárate, L., Doane, A. S., Li, Z., Verma, A., Paiva, B., Martín-Subero, J. I., Elemento, O., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08679-z · Cited by 98 · see citing works
Self-citationKang, J., Kim, J., Kim, K., Park, J. W., Cho, H., Hahm, J. Y., Chae, Y., Kim, D., Kook, H. Y., Rhee, S., et al. (2018) · The FASEB Journal · doi:10.1096/fj.201800242r · Cited by 97 · see citing works
Ramakrishnan, S., Granger, V., Rak, M., Hu, Q., Attwood, K. M., Aquila, L., Krishnan, N., Osiecki, R., Azabdaftari, G., Guru, K. A., et al. (2019) · Cell Death and Differentiation · doi:10.1038/s41418-019-0278-9 · Cited by 94 · see citing works
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Hatzi, K., Geng, H., Doane, A. S., Meydan, C., LaRiviere, R., Cárdenas, M., Duy, C., Shen, H., Calvo-Vidal, M. N., Baslan, T., et al. (2018) · Nature Immunology · doi:10.1038/s41590-018-0273-1 · Cited by 93 · see citing works
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Zhang, C. Z., Chen, S.-L., Wang, C., He, Y.-F., Yang, X., Xie, D., & Yun, J. (2017) · Cancer Research · doi:10.1158/0008-5472.can-17-0700 · Cited by 91 · see citing works
BAHCC1 binds H3K27me3 via a conserved BAH module to mediate gene silencing and oncogenesis
Fan, H., Lu, J., Guo, Y., Li, D., Zhang, Z., Tsai, Y., Pi, W., Ahn, J. H., Gong, W., Xiang, Y., et al. (2020) · Nature Genetics · doi:10.1038/s41588-020-00729-3 · Cited by 90 · see citing works
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Yin, Y., Qiu, S., Li, X., Huang, B., Xu, Y., & Peng, Y. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0993-4 · Cited by 89 · see citing works
Polycomb complexes PRC1 and their function in hematopoiesis
Vidal, M., & Starowicz, K. (2017) · Experimental Hematology · doi:10.1016/j.exphem.2016.12.006 · Cited by 83 · see citing works
BCL6 as a therapeutic target for lymphoma
Leeman‐Neill, R. J., & Bhagat, G. (2017) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2018.1420782 · Cited by 85 · see citing works
Wang, S., Denton, K. E., Hobbs, K., Weaver, T., McFarlane, J. M. B., Connelly, K. E., Gignac, M. C., Milosevich, N., Hof, F. A., Paci, I., et al. (2019) · ACS Chemical Biology · doi:10.1021/acschembio.9b00654 · Cited by 85 · see citing works
Julia, E., & Salles, G. (2021) · Future Oncology · doi:10.2217/fon-2020-1244 · Cited by 79 · see citing works
Isshiki, Y., Chen, X., Teater, M. R., Karagiannidis, I., Nam, H. S., Cai, W., Meydan, C., Xia, M., Shen, H., Gutierrez, J., et al. (2024) · Cancer Cell · doi:10.1016/j.ccell.2024.11.006 · Cited by 84 · see citing works
Self-citationEpigenetic regulation of B cells and its role in autoimmune pathogenesis
Xiao, F., Rui, K., Shi, X., Wu, H., Cai, X., Lui, K. O., Lu, Q., Ballestar, E., Tian, J., Zou, H., et al. (2022) · Cellular and Molecular Immunology · doi:10.1038/s41423-022-00933-7 · Cited by 78 · see citing works
Zhu, F., Guo, H., Bates, P. D., Zhang, S., Zhang, H., Nomie, K. J., Li, Y., Lü, L., Seibold, K. R., Wang, F., et al. (2019) · Leukemia · doi:10.1038/s41375-019-0489-6 · Cited by 77 · see citing works
Brach, D., Johnston-Blackwell, D., Drew, A., Lingaraj, T., Motwani, V., Warholic, N. M., Feldman, I., Plescia, C., Smith, J. J., Copeland, R. A., et al. (2017) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-16-0840 · Cited by 70 · see citing works
BCOR gene alterations in hematologic diseases
Sportoletti, P., Sorcini, D., & Falini, B. (2021) · Blood · doi:10.1182/blood.2021010958 · Cited by 67 · see citing works
Bcor loss perturbs myeloid differentiation and promotes leukaemogenesis
Kelly, M. J., So, J., Rogers, A. J., Gregory, G. P., Li, J., Zethoven, M., Gearhart, M. D., Bardwell, V. J., Johnstone, R. W., Vervoort, S. J., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09250-6 · Cited by 65 · see citing works
Self-citationMolecular regulation of peripheral B cells and their progeny in immunityPreprint
Boothby, M. R., Hodges, E. C., & Thomas, J. W. (2019) · Genes & Development · doi:10.1101/gad.320192.118 · Cited by 65 · see citing works
Polycomb complexes in normal and malignant hematopoiesis
Carlo, V. D., Mocavini, I., & Croce, L. D. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201808028 · Cited by 61 · see citing works
Internal deletion of BCOR reveals a tumor suppressor function for BCOR in T lymphocyte malignancies
Tanaka, T. N., Nakajima‐Takagi, Y., Aoyama, K., Tara, S., Oshima, M., Saraya, A., Koide, S., Si, S., Manabe, I., Sanada, M., et al. (2017) · The Journal of Experimental Medicine · doi:10.1084/jem.20170167 · Cited by 62 · see citing works
Purwada, A., Shah, S. B., Béguelin, W., August, A., Melnick, A. M., & Singh, A. K. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.06.034 · Cited by 60 · see citing works
Self-citationBujisic, B., Gassart, A. D., Tallant, R., Demaria, O., Zaffalon, L., Chelbi, S. T., Gilliet, M. F., Bertoni, F., & Martinon, F. (2017) · Blood · doi:10.1182/blood-2016-09-741348 · Cited by 60 · see citing works
Wang, S., Alpsoy, A., Sood, S., Ordonez‐Rubiano, S. C., Dhiman, A., Sun, Y., Jiao, G., Krusemark, C. J., & Dykhuizen, E. C. (2021) · ChemBioChem · doi:10.1002/cbic.202100118 · Cited by 58 · see citing works
Polycomb repressive complexes in hematological malignancies
Iwama, A. (2017) · Blood · doi:10.1182/blood-2017-02-739490 · Cited by 55 · see citing works
Robustness of In Vitro Selection Assays of DNA-Encoded Peptidomimetic Ligands to CBX7 and CBX8
Denton, K. E., Wang, S., Gignac, M. C., Milosevich, N., Hof, F. A., Dykhuizen, E. C., & Krusemark, C. J. (2018) · SLAS DISCOVERY · doi:10.1177/2472555217750871 · Cited by 55 · see citing works
Multifaceted role of the polycomb-group gene EZH2 in hematological malignancies
Sashida, G., & Iwama, A. (2016) · International Journal of Hematology · doi:10.1007/s12185-016-2124-x · Cited by 52 · see citing works
Ding, S., Zhang, Q., Luo, S., Gao, L., Huang, J., Lu, J., Chen, J., Zeng, Q., Guo, A., Zeng, J., et al. (2019) · Cellular and Molecular Immunology · doi:10.1038/s41423-019-0268-3 · Cited by 48 · see citing works
Epigenetic Programing of B-Cell Lymphoma by BCL6 and Its Genetic Deregulation
Yang, H., & Green, M. R. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00272 · Cited by 48 · see citing works
Frequent mutations in the amino-terminal domain of BCL7A impair its tumor suppressor role in DLBCL
Baliñas-Gavira, C., Rodríguez, M. I., Andrades, Á., Cuadros, M., Álvarez-Pérez, J. C., Álvarez-Prado, Á. F., de Yébenes, V. G., Sánchez-Hernández, S., Fernández-Vigo, E., Muñoz, J., et al. (2020) · Leukemia · doi:10.1038/s41375-020-0919-5 · Cited by 48 · see citing works
BCL6 confers KRAS-mutant non–small-cell lung cancer resistance to BET inhibitors
Guo, J., Liu, Y., Lv, J., Zou, B., Chen, Z., Li, K., Feng, J., Cai, Z., Wei, L., Liu, M., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci133090 · Cited by 47 · see citing works
Epigenetic regulation of B cell fate and function during an immune response
Zhang, Y., & Good‐Jacobson, K. L. (2019) · Immunological Reviews · doi:10.1111/imr.12733 · Cited by 48 · see citing works
Polycomb Repressor Complex 2 in Genomic Instability and Cancer
Veneti, Z., Gkouskou, K. K., & Eliopoulos, A. G. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18081657 · Cited by 45 · see citing works
Histone methyltransferase DOT1L controls state-specific identity during B cell differentiation
Aslam, M. A., Alemdehy, M. F., Kwesi‐Maliepaard, E. M., Cagánová, M., Pardieck, I. N., van den Brand, T., Muhaimin, F. I., van Welsem, T., de Rink, I., Song, J., et al. (2021) · EMBO Reports · doi:10.15252/embr.202051184 · Cited by 43 · see citing works
Schaefer, E. J., Wang, H. C., Karp, H. Q., Meyer, C. A., Cejas, P., Gearhart, M. D., Adelman, E. R., Fares, I., Apffel, A. M., Lim, K., et al. (2021) · Blood Cancer Discovery · doi:10.1158/2643-3230.bcd-21-0115 · Cited by 42 · see citing works
Self-citationCompositional and functional diversity of canonical PRC1 complexes in mammals
Connelly, K. E., & Dykhuizen, E. C. (2016) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2016.12.006 · Cited by 44 · see citing works
BCL6 maintains survival and self-renewal of primary human acute myeloid leukemia cells
Kawabata, K. C., Zong, H., Meydan, C., Wyman, S., Wouters, B. J., Sugita, M., Goswami, S., Albert, M., Yip, W., Roboz, G. J., et al. (2020) · Blood · doi:10.1182/blood.2019001745 · Cited by 42 · see citing works
Self-citationLi, J., Chin, C. R., Ying, H., Meydan, C., Teater, M. R., Xia, M., Farinha, P., Takata, K., Chu, C.-S., Jiang, Y., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-47012-1 · Cited by 44 · see citing works
Self-citationGood‐Jacobson, K. L. (2018) · Immunological Reviews · doi:10.1111/imr.12663 · Cited by 40 · see citing works
Pietro, A. D., Polmear, J., Cooper, L., Damelang, T., Hussain, T., Hailes, L., O’Donnell, K., Udupa, V., Tian, M., Preston, S., et al. (2021) · Nature Immunology · doi:10.1038/s41590-021-01077-y · Cited by 40 · see citing works
Sjögren's syndrome X‐chromosome dose effect: An epigenetic perspective
Mougeot, J., Noll, B. D., & Mougeot, F. B. (2018) · Oral Diseases · doi:10.1111/odi.12825 · Cited by 39 · see citing works
BCL6 is regulated by the MAPK/ELK1 axis and promotes KRAS-driven lung cancer
Li, K., Liu, Y., Ding, Y., Zhang, Z., Feng, J., Hu, J., Chen, J., Lian, Z., Chen, Y., Hu, K., et al. (2022) · Journal of Clinical Investigation · doi:10.1172/jci161308 · Cited by 37 · see citing works
Epigenetic regulation of chemokine ( CC ‐motif) ligand 2 in inflammatory diseases
Chen, Y., Liu, S., Wu, L., Liu, Y., Du, J., Luo, Z., Xu, J., Guo, L., & Liu, Y. F. (2023) · Cell Proliferation · doi:10.1111/cpr.13428 · Cited by 36 · see citing works
UTX Regulates Human Neural Differentiation and Dendritic Morphology by Resolving Bivalent Promoters
Tang, Q.-Y., Zhang, S.-F., Dai, S., Liu, C., Wang, Y.-Y., Du, H.-Z., Teng, Z., & Liu, C. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.06.015 · Cited by 34 · see citing works
Charting the dynamic epigenome during B-cell development
Martín-Subero, J. I., & Oakes, C. C. (2017) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2017.08.008 · Cited by 35 · see citing works
Soshnev, A. A., Allis, C. D., Cesarman, E., & Melnick, A. M. (2021) · Cancer Research · doi:10.1158/0008-5472.can-21-2619 · Cited by 30 · see citing works
Self-citationMolecular Subgroups of Diffuse Large B Cell Lymphoma: Biology and Implications for Clinical Practice
Weber, T., & Schmitz, R. (2022) · Current Oncology Reports · doi:10.1007/s11912-021-01155-2 · Cited by 33 · see citing works
Peeters, J. G. C., Silveria, S. L., Özdemir, M., Ramachandran, S., & DuPage, M. J. P. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114724 · Cited by 30 · see citing works
Chikada, H., Ida, K., Ando, E., Inagaki, Y., Sakamoto, A., & Kamiya, A. (2018) · Laboratory Investigation · doi:10.1038/s41374-018-0088-6 · Cited by 31 · see citing works
Dolcino, M., Tinazzi, E., Vitali, C., Papa, N. D., Puccetti, A., & Lunardi, C. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8091349 · Cited by 31 · see citing works
Zeng, F., Luo, L., Li, D., Guo, J., & Guo, M. (2021) · Journal of Translational Medicine · doi:10.1186/s12967-021-02709-5 · Cited by 31 · see citing works
Yan, Z., Ao, X., Liang, X., Chen, Z., Liu, Y., Wang, P., Wang, D., Liu, Z., Liu, X., Zhu, J., et al. (2022) · Respiratory Research · doi:10.1186/s12931-022-02024-7 · Cited by 31 · see citing works
Zhou, J., Nie, D., Li, J., Du, X., Lu, Y., Li, Y., Liu, C., Dai, W., Wang, Y., Jin, Y., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-1533 · Cited by 30 · see citing works
The Pathologic and Genetic Characteristics of Extranodal NK/T-Cell Lymphoma
Kim, H., & Ko, Y. H. (2022) · Life · doi:10.3390/life12010073 · Cited by 30 · see citing works
Polycomb Directed Cell Fate Decisions in Development and Cancer
German, B., & Ellis, L. (2022) · Epigenomes · doi:10.3390/epigenomes6030028 · Cited by 36 · see citing works
Serganova, I. S., Chakraborty, S., Yamshon, S., Isshiki, Y., Bucktrout, R., Melnick, A. M., Béguelin, W., & Zappasodi, R. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.805195 · Cited by 29 · see citing works
Self-citationGu, H., He, J., Li, Y., Mi, D., Guan, T., Guo, W., Liu, B., & Chen, Y. (2022) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.2c01433 · Cited by 29 · see citing works
Alzrigat, M., Párraga, A. A., Majumder, M. M., Ma, A., Jin, J. J., Österborg, A., Nahi, H., Nilsson, K., Heckman, C. A., Oberg, F. G., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.21909 · Cited by 28 · see citing works
New players in the gene regulatory network controlling late B cell differentiation
Willis, S. N., & Nutt, S. L. (2019) · Current Opinion in Immunology · doi:10.1016/j.coi.2019.04.007 · Cited by 27 · see citing works
Xing, Y., Guo, W., Wu, M. Y., Xie, J., Huang, D., Hu, P., Zhou, M., Zhang, L., Zhang, Q., Wang, P., et al. (2022) · Cancer Letters · doi:10.1016/j.canlet.2021.12.035 · Cited by 28 · see citing works
Clinical advances in epigenetic therapies for lymphoma
Rosenthal, A. C., Munoz, J. L., & Villasboas, J. C. (2023) · Clinical Epigenetics · doi:10.1186/s13148-023-01452-6 · Cited by 28 · see citing works
Taming the Heterogeneity of Aggressive Lymphomas for Precision Therapy
Young, R. M., Phelan, J. D., Shaffer, A. L., Wright, G. W., Huang, D. W., Schmitz, R., Johnson, C. A., Oellerich, T., Wilson, W. H., & Staudt, L. M. (2018) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-030518-055734 · Cited by 28 · see citing works
Cramer, S., Li, R., Ali, S. M., Bradley, J. A., Kim, H. K., & Pressey, J. G. (2017) · Journal of the National Comprehensive Cancer Network · doi:10.6004/jnccn.2017.0124 · Cited by 27 · see citing works
Epigenetic Reprogramming and Emerging Epigenetic Therapies in CML
Bugler, J., Kinstrie, R., Scott, M. T., & Vetrie, D. L. P. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00136 · Cited by 27 · see citing works
Romero, P., Richart, L., Aflaki, S., Petitalot, A., Burton, M., Michaud, A., Masliah‐Planchon, J., Kuhnowski, F., Cam, S. L., Baliñas-Gavira, C., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-47701-x · Cited by 26 · see citing works
Zhang, S., Lin, S., Tang, Q., & Yan, Z. (2021) · Molecular Medicine Reports · doi:10.3892/mmr.2021.12458 · Cited by 24 · see citing works
Reprogramming CBX8-PRC1 function with a positive allosteric modulator
Suh, J. L., Bsteh, D., Hart, B., Si, Y., Weaver, T., Pribitzer, C., Lau, R., Soni, S., Ogana, H. A. N., Rectenwald, J. M., et al. (2021) · Cell chemical biology · doi:10.1016/j.chembiol.2021.10.003 · Cited by 26 · see citing works
Roadmap to a plasma cell: Epigenetic and transcriptional cues that guide B cell differentiation
Wiggins, K. J., & Scharer, C. D. (2020) · Immunological Reviews · doi:10.1111/imr.12934 · Cited by 29 · see citing works
Chen, Y., Xu, R., Ruze, R., Yang, J., Wang, H., Song, J., You, L., Wang, C., & Zhao, Y. (2021) · Cancer Cell International · doi:10.1186/s12935-021-01928-6 · Cited by 25 · see citing works
Taking the EZ way: Targeting enhancer of zeste homolog 2 in B-cell lymphomas
Morschhauser, F., Salles, G., Batlevi, C. L., Tilly, H., Chaidos, A., Phillips, T., Burke, J. M., & Melnick, A. M. (2022) · Blood Reviews · doi:10.1016/j.blre.2022.100988 · Cited by 25 · see citing works
Self-citation
- Authors
- Béguelin, W., Teater, M., Gearhart, M. D., Calvo Fernández, M. T., Goldstein, R. L., Cárdenas, M. G., Hatzi, K., Rosen, M., Shen, H., Corcoran, C. M., Hamline, M. Y., Gascoyne, R. D., Levine, R. L., Abdel-Wahab, O., Licht, J. D., Shaknovich, R., Elemento, O., Bardwell, V. J., & Melnick, A. M.
- Affiliations
- Cornell University (US)
- University of Minnesota (US)
- BC Cancer Agency (CA)
- Memorial Sloan Kettering Cancer Center (US)
- Northwestern University (US)
- Corresponding author
- Bardwell, Vivian J.
- Melnick, Ari M.
- ORCID
- Venue
- Cancer Cell
- Publisher
- Elsevier BV
- Published
- 2016-08
- Volume
- 30
- Issue
- 2
- Pages
- 197-213
- ISSN
- 1535-6108 (ISSN-L)
- PMC
- PMC5000552
- OpenAlex
- W2515546929
- Cited by
- 254
- References
- 42
- Citations by year
- 2026: 14 · 2025: 19 · 2024: 17 · 2023: 20 · 2022: 23 · 2021: 40 · 2020: 34 · 2019: 31 · 2018: 28 · 2017: 24 · 2016: 4
- FWCI
- 15.08
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 372 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cancer Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health (5F30HL093996, 5T32GM008244, AHA 0810194Z)
- National Cancer Institute (R01 CA071540)
- American Society of Hematology
- Leukemia and Lymphoma Society (TRP 6141-14)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Pathology and Forensic Medicine › Lymphoma Diagnosis and Treatment
- Keywords
- EZH2, BCL6, CBX8, BCOR, PRC1, bivalent promoters, H3K27me3, germinal center formation, diffuse large B-cell lymphoma, lymphomagenesis, histone methyltransferase, chromodomain protein, histone modifications, combination therapy
- MeSH terms
- Enhancer of Zeste Homolog 2 Protein, Animals, Humans, Mice, Inbred C57BL, Mice, Transgenic, Promoter Regions, Genetic, Proto-Oncogene Proteins, Repressor Proteins, Transcription, Genetic, Lymphoma, Large B-Cell, Diffuse, Germinal Center, Mitochondrial Membrane Transport Proteins, Mice, Proto-Oncogene Proteins c-bcl-6, Polycomb-Group Proteins, Polycomb Repressive Complex 1
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