BET and HDAC inhibitors induce similar genes and biological effects and synergize to kill in Myc-induced murine lymphoma
The bromodomain and extraterminal (BET) domain family of proteins binds to acetylated lysines on histones and regulates gene transcription. Recently, BET inhibitors (BETi) have been developed that show promise as potent anticancer drugs against various solid and hematological malignancies. Here we s...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2014-07, Vol.111 (26), p.E2721-E2730 |
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| creator | Bhadury, Joydeep Nilsson, Lisa M Muralidharan, Somsundar Veppil Green, Lydia C Li, Zhoulei Gesner, Emily M Hansen, Henrik C Keller, Ulrich B McLure, Kevin G Nilsson, Jonas A |
| description | The bromodomain and extraterminal (BET) domain family of proteins binds to acetylated lysines on histones and regulates gene transcription. Recently, BET inhibitors (BETi) have been developed that show promise as potent anticancer drugs against various solid and hematological malignancies. Here we show that the structurally novel and orally bioavailable BET inhibitor RVX2135 inhibits proliferation and induces apoptosis of lymphoma cells arising in Myc-transgenic mice in vitro and in vivo. We find that BET inhibition exhibits broad transcriptional effects in Myc-transgenic lymphoma cells affecting many transcription factor networks. By examining the genes induced by BETi, which have largely been ignored to date, we discovered that these were similar to those induced by histone deacetylase inhibitors (HDACi). HDACi also induced cell-cycle arrest and cell death of Myc-induced murine lymphoma cells and synergized with BETi. Our data suggest that BETi sensitize Myc-overexpressing lymphoma cells partly by inducing HDAC-silenced genes, and suggest synergistic and therapeutic combinations by targeting the genetic link between BETi and HDACi. |
| doi_str_mv | 10.1073/pnas.1406722111 |
| format | Article |
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Recently, BET inhibitors (BETi) have been developed that show promise as potent anticancer drugs against various solid and hematological malignancies. Here we show that the structurally novel and orally bioavailable BET inhibitor RVX2135 inhibits proliferation and induces apoptosis of lymphoma cells arising in Myc-transgenic mice in vitro and in vivo. We find that BET inhibition exhibits broad transcriptional effects in Myc-transgenic lymphoma cells affecting many transcription factor networks. By examining the genes induced by BETi, which have largely been ignored to date, we discovered that these were similar to those induced by histone deacetylase inhibitors (HDACi). HDACi also induced cell-cycle arrest and cell death of Myc-induced murine lymphoma cells and synergized with BETi. Our data suggest that BETi sensitize Myc-overexpressing lymphoma cells partly by inducing HDAC-silenced genes, and suggest synergistic and therapeutic combinations by targeting the genetic link between BETi and HDACi.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1406722111</identifier><identifier>PMID: 24979794</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>ACUTE ; ACUTE MYELOID-LEUKEMIA ; Animals ; antineoplastic agents ; Apoptosis ; Apoptosis - drug effects ; B-CELL LYMPHOMA ; Biological Sciences ; Brd2 ; Brd4 ; BROMODOMAIN PROTEIN BRD4 ; C-MYC ; Cancer and Oncology ; Cancer och onkologi ; Cancer therapies ; Cell cycle ; DISRUPTION ; Drug Synergism ; Gene Expression Regulation, Neoplastic - drug effects ; gene overexpression ; genes ; histone deacetylase ; HISTONE DEACETYLASE INHIBITORS ; Histone Deacetylase Inhibitors - pharmacology ; histones ; JQ1 ; LYMPHOBLASTIC-LEUKEMIA ; Lymphoma ; Medical Genetics and Genomics ; Medicinsk genetik och genomik ; Mice ; Mice, Transgenic ; mouse models ; neoplasm cells ; Nerve Tissue Proteins - antagonists & inhibitors ; P-TEFB ; PNAS Plus ; Proteins ; Quinazolinones - pharmacology ; Receptors, Cell Surface - antagonists & inhibitors ; SELECTIVE-INHIBITION ; transcription (genetics) ; transcription factors ; Transcription Factors - metabolism ; TRANSCRIPTIONAL ELONGATION ; vorinostat</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2014-07, Vol.111 (26), p.E2721-E2730</ispartof><rights>Copyright National Academy of Sciences Jul 1, 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c640t-c7ecae6ad7807941b9bca1a2ae0196677bad30f04250d5f036b4f24a2791a3e83</citedby><cites>FETCH-LOGICAL-c640t-c7ecae6ad7807941b9bca1a2ae0196677bad30f04250d5f036b4f24a2791a3e83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/111/26.cover.gif</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4084424/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4084424/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24979794$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://gup.ub.gu.se/publication/200919$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Bhadury, Joydeep</creatorcontrib><creatorcontrib>Nilsson, Lisa M</creatorcontrib><creatorcontrib>Muralidharan, Somsundar Veppil</creatorcontrib><creatorcontrib>Green, Lydia C</creatorcontrib><creatorcontrib>Li, Zhoulei</creatorcontrib><creatorcontrib>Gesner, Emily M</creatorcontrib><creatorcontrib>Hansen, Henrik C</creatorcontrib><creatorcontrib>Keller, Ulrich B</creatorcontrib><creatorcontrib>McLure, Kevin G</creatorcontrib><creatorcontrib>Nilsson, Jonas A</creatorcontrib><title>BET and HDAC inhibitors induce similar genes and biological effects and synergize to kill in Myc-induced murine lymphoma</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The bromodomain and extraterminal (BET) domain family of proteins binds to acetylated lysines on histones and regulates gene transcription. Recently, BET inhibitors (BETi) have been developed that show promise as potent anticancer drugs against various solid and hematological malignancies. Here we show that the structurally novel and orally bioavailable BET inhibitor RVX2135 inhibits proliferation and induces apoptosis of lymphoma cells arising in Myc-transgenic mice in vitro and in vivo. We find that BET inhibition exhibits broad transcriptional effects in Myc-transgenic lymphoma cells affecting many transcription factor networks. By examining the genes induced by BETi, which have largely been ignored to date, we discovered that these were similar to those induced by histone deacetylase inhibitors (HDACi). HDACi also induced cell-cycle arrest and cell death of Myc-induced murine lymphoma cells and synergized with BETi. Our data suggest that BETi sensitize Myc-overexpressing lymphoma cells partly by inducing HDAC-silenced genes, and suggest synergistic and therapeutic combinations by targeting the genetic link between BETi and HDACi.</description><subject>ACUTE</subject><subject>ACUTE MYELOID-LEUKEMIA</subject><subject>Animals</subject><subject>antineoplastic agents</subject><subject>Apoptosis</subject><subject>Apoptosis - drug effects</subject><subject>B-CELL LYMPHOMA</subject><subject>Biological Sciences</subject><subject>Brd2</subject><subject>Brd4</subject><subject>BROMODOMAIN PROTEIN BRD4</subject><subject>C-MYC</subject><subject>Cancer and Oncology</subject><subject>Cancer och onkologi</subject><subject>Cancer therapies</subject><subject>Cell cycle</subject><subject>DISRUPTION</subject><subject>Drug Synergism</subject><subject>Gene Expression Regulation, Neoplastic - drug effects</subject><subject>gene overexpression</subject><subject>genes</subject><subject>histone deacetylase</subject><subject>HISTONE DEACETYLASE INHIBITORS</subject><subject>Histone Deacetylase Inhibitors - pharmacology</subject><subject>histones</subject><subject>JQ1</subject><subject>LYMPHOBLASTIC-LEUKEMIA</subject><subject>Lymphoma</subject><subject>Medical Genetics and Genomics</subject><subject>Medicinsk genetik och genomik</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>mouse models</subject><subject>neoplasm cells</subject><subject>Nerve Tissue Proteins - antagonists & inhibitors</subject><subject>P-TEFB</subject><subject>PNAS Plus</subject><subject>Proteins</subject><subject>Quinazolinones - pharmacology</subject><subject>Receptors, Cell Surface - antagonists & inhibitors</subject><subject>SELECTIVE-INHIBITION</subject><subject>transcription (genetics)</subject><subject>transcription factors</subject><subject>Transcription Factors - metabolism</subject><subject>TRANSCRIPTIONAL ELONGATION</subject><subject>vorinostat</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk1v1DAQhiMEokvhzA0sceGSdsbxOskFqSwLRSriQHu2HGeSdUnixU6A5dfjJctCuSAfbI2feTUfb5I8RThDyLPz7aDDGQqQOeeIeC9ZIJSYSlHC_WQBwPO0EFycJI9CuAWAclnAw-SEizKPRyyS76_X10wPNbt8c7FidtjYyo7Oh_isJ0Ms2N522rOWBgq_wMq6zrXW6I5R05AZ53DYDeRb-4PY6Nhn23VRgX3YmXQWqlk_eTsQ63b9duN6_Th50Ogu0JPDfZrcvF1fry7Tq4_v3q8urlIjBYypyclokrrOC4gFY1VWRqPmmgBLKfO80nUGDQi-hHrZQCYr0XCheV6izqjITpN01g3faDtVauttr_1OOW1VO21VDLWTCqR4nA6WkX818xHuqTY0jF53d9Lu_gx2o1r3VQkoRBx1FHh5EPDuy0RhVL0NhrpOD-SmoLCADONmSvl_dLlEKTKOENEX_6C3bvJDnFykhBBxs7CnzmfKeBeCp-ZYN4LaG0btDaP-GCZmPPu73SP_2yERYAdgn3mUQ1RcqjXP-V7j-Yw02indehvUzScOKAEwViaK7CdxMNC-</recordid><startdate>20140701</startdate><enddate>20140701</enddate><creator>Bhadury, Joydeep</creator><creator>Nilsson, Lisa M</creator><creator>Muralidharan, Somsundar Veppil</creator><creator>Green, Lydia C</creator><creator>Li, Zhoulei</creator><creator>Gesner, Emily M</creator><creator>Hansen, Henrik C</creator><creator>Keller, Ulrich B</creator><creator>McLure, Kevin G</creator><creator>Nilsson, Jonas A</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>F1U</scope></search><sort><creationdate>20140701</creationdate><title>BET and HDAC inhibitors induce similar genes and biological effects and synergize to kill in Myc-induced murine lymphoma</title><author>Bhadury, Joydeep ; Nilsson, Lisa M ; Muralidharan, Somsundar Veppil ; Green, Lydia C ; Li, Zhoulei ; Gesner, Emily M ; Hansen, Henrik C ; Keller, Ulrich B ; McLure, Kevin G ; Nilsson, Jonas A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c640t-c7ecae6ad7807941b9bca1a2ae0196677bad30f04250d5f036b4f24a2791a3e83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>ACUTE</topic><topic>ACUTE MYELOID-LEUKEMIA</topic><topic>Animals</topic><topic>antineoplastic agents</topic><topic>Apoptosis</topic><topic>Apoptosis - drug effects</topic><topic>B-CELL LYMPHOMA</topic><topic>Biological Sciences</topic><topic>Brd2</topic><topic>Brd4</topic><topic>BROMODOMAIN PROTEIN BRD4</topic><topic>C-MYC</topic><topic>Cancer and Oncology</topic><topic>Cancer och onkologi</topic><topic>Cancer therapies</topic><topic>Cell cycle</topic><topic>DISRUPTION</topic><topic>Drug Synergism</topic><topic>Gene Expression Regulation, Neoplastic - drug effects</topic><topic>gene overexpression</topic><topic>genes</topic><topic>histone deacetylase</topic><topic>HISTONE DEACETYLASE INHIBITORS</topic><topic>Histone Deacetylase Inhibitors - pharmacology</topic><topic>histones</topic><topic>JQ1</topic><topic>LYMPHOBLASTIC-LEUKEMIA</topic><topic>Lymphoma</topic><topic>Medical Genetics and Genomics</topic><topic>Medicinsk genetik och genomik</topic><topic>Mice</topic><topic>Mice, Transgenic</topic><topic>mouse models</topic><topic>neoplasm cells</topic><topic>Nerve Tissue Proteins - antagonists & inhibitors</topic><topic>P-TEFB</topic><topic>PNAS Plus</topic><topic>Proteins</topic><topic>Quinazolinones - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Göteborgs universitet</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bhadury, Joydeep</au><au>Nilsson, Lisa M</au><au>Muralidharan, Somsundar Veppil</au><au>Green, Lydia C</au><au>Li, Zhoulei</au><au>Gesner, Emily M</au><au>Hansen, Henrik C</au><au>Keller, Ulrich B</au><au>McLure, Kevin G</au><au>Nilsson, Jonas A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>BET and HDAC inhibitors induce similar genes and biological effects and synergize to kill in Myc-induced murine lymphoma</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2014-07-01</date><risdate>2014</risdate><volume>111</volume><issue>26</issue><spage>E2721</spage><epage>E2730</epage><pages>E2721-E2730</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>The bromodomain and extraterminal (BET) domain family of proteins binds to acetylated lysines on histones and regulates gene transcription. Recently, BET inhibitors (BETi) have been developed that show promise as potent anticancer drugs against various solid and hematological malignancies. Here we show that the structurally novel and orally bioavailable BET inhibitor RVX2135 inhibits proliferation and induces apoptosis of lymphoma cells arising in Myc-transgenic mice in vitro and in vivo. We find that BET inhibition exhibits broad transcriptional effects in Myc-transgenic lymphoma cells affecting many transcription factor networks. By examining the genes induced by BETi, which have largely been ignored to date, we discovered that these were similar to those induced by histone deacetylase inhibitors (HDACi). HDACi also induced cell-cycle arrest and cell death of Myc-induced murine lymphoma cells and synergized with BETi. Our data suggest that BETi sensitize Myc-overexpressing lymphoma cells partly by inducing HDAC-silenced genes, and suggest synergistic and therapeutic combinations by targeting the genetic link between BETi and HDACi.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>24979794</pmid><doi>10.1073/pnas.1406722111</doi><oa>free_for_read</oa></addata></record> |
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| source | Jstor Complete Legacy; MEDLINE; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
| subjects | ACUTE ACUTE MYELOID-LEUKEMIA Animals antineoplastic agents Apoptosis Apoptosis - drug effects B-CELL LYMPHOMA Biological Sciences Brd2 Brd4 BROMODOMAIN PROTEIN BRD4 C-MYC Cancer and Oncology Cancer och onkologi Cancer therapies Cell cycle DISRUPTION Drug Synergism Gene Expression Regulation, Neoplastic - drug effects gene overexpression genes histone deacetylase HISTONE DEACETYLASE INHIBITORS Histone Deacetylase Inhibitors - pharmacology histones JQ1 LYMPHOBLASTIC-LEUKEMIA Lymphoma Medical Genetics and Genomics Medicinsk genetik och genomik Mice Mice, Transgenic mouse models neoplasm cells Nerve Tissue Proteins - antagonists & inhibitors P-TEFB PNAS Plus Proteins Quinazolinones - pharmacology Receptors, Cell Surface - antagonists & inhibitors SELECTIVE-INHIBITION transcription (genetics) transcription factors Transcription Factors - metabolism TRANSCRIPTIONAL ELONGATION vorinostat |
| title | BET and HDAC inhibitors induce similar genes and biological effects and synergize to kill in Myc-induced murine lymphoma |
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