Aberrant Overexpression of IL-15 Initiates Large Granular Lymphocyte Leukemia through Chromosomal Instability and DNA Hypermethylation
How inflammation causes cancer is unclear. Interleukin-15 (IL-15) is a pro-inflammatory cytokine elevated in human large granular lymphocyte (LGL) leukemia. Mice overexpressing IL-15 develop LGL leukemia. Here, we show that prolonged in vitro exposure of wild-type (WT) LGL to IL-15 results in Myc-me...
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| Veröffentlicht in: | Cancer cell 2012-11, Vol.22 (5), p.645-655 |
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| creator | Mishra, Anjali Liu, Shujun Sams, Gregory H. Curphey, Douglas P. Santhanam, Ramasamy Rush, Laura J. Schaefer, Deanna Falkenberg, Lauren G. Sullivan, Laura Jaroncyk, Laura Yang, Xiaojuan Fisk, Harold Wu, Lai-Chu Hickey, Christopher Chandler, Jason C. Wu, Yue-Zhong Heerema, Nyla A. Chan, Kenneth K. Perrotti, Danilo Zhang, Jianying Porcu, Pierluigi Racke, Frederick K. Garzon, Ramiro Lee, Robert J. Marcucci, Guido Caligiuri, Michael A. |
| description | How inflammation causes cancer is unclear. Interleukin-15 (IL-15) is a pro-inflammatory cytokine elevated in human large granular lymphocyte (LGL) leukemia. Mice overexpressing IL-15 develop LGL leukemia. Here, we show that prolonged in vitro exposure of wild-type (WT) LGL to IL-15 results in Myc-mediated upregulation of aurora kinases, centrosome aberrancies, and aneuploidy. Simultaneously, IL-15 represses miR-29b via induction of Myc/NF-κBp65/Hdac-1, resulting in Dnmt3b overexpression and DNA hypermethylation. All this is validated in human LGL leukemia. Adoptive transfer of WT LGL cultured with IL-15 led to malignant transformation in vivo. Drug targeting that reverses miR-29b repression cures otherwise fatal LGL leukemia. We show how excessive IL-15 initiates cancer and demonstrate effective drug targeting for potential therapy of human LGL leukemia.
► A single pro-inflammatory cytokine, IL-15, can initiate malignant transformation ► IL-15-mediated induction of Myc is central to the genesis of leukemia ► Targeting miR-29b with a single therapeutic induces long-term remission of leukemia |
| doi_str_mv | 10.1016/j.ccr.2012.09.009 |
| format | Article |
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► A single pro-inflammatory cytokine, IL-15, can initiate malignant transformation ► IL-15-mediated induction of Myc is central to the genesis of leukemia ► Targeting miR-29b with a single therapeutic induces long-term remission of leukemia</description><identifier>ISSN: 1535-6108</identifier><identifier>EISSN: 1878-3686</identifier><identifier>DOI: 10.1016/j.ccr.2012.09.009</identifier><identifier>PMID: 23153537</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Aneuploidy ; Animals ; Cell Transformation, Neoplastic - genetics ; Centrosome - physiology ; Chromosomal Instability ; Chromosome Segregation ; DNA (Cytosine-5-)-Methyltransferases - genetics ; DNA (Cytosine-5-)-Methyltransferases - metabolism ; DNA Methylation ; DNA Methyltransferase 3B ; Gene Expression Regulation, Neoplastic ; Humans ; Interleukin-15 - genetics ; Interleukin-15 - metabolism ; Leukemia, Large Granular Lymphocytic - genetics ; Leukemia, Large Granular Lymphocytic - metabolism ; Mice ; MicroRNAs - genetics ; MicroRNAs - metabolism</subject><ispartof>Cancer cell, 2012-11, Vol.22 (5), p.645-655</ispartof><rights>2012 Elsevier Inc.</rights><rights>Copyright © 2012 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c517t-f192542527d380a2a236b59498583f0cd1053420eeebb158e4d156c6059d807d3</citedby><cites>FETCH-LOGICAL-c517t-f192542527d380a2a236b59498583f0cd1053420eeebb158e4d156c6059d807d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ccr.2012.09.009$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3536,27903,27904,45974</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23153537$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mishra, Anjali</creatorcontrib><creatorcontrib>Liu, Shujun</creatorcontrib><creatorcontrib>Sams, Gregory H.</creatorcontrib><creatorcontrib>Curphey, Douglas P.</creatorcontrib><creatorcontrib>Santhanam, Ramasamy</creatorcontrib><creatorcontrib>Rush, Laura J.</creatorcontrib><creatorcontrib>Schaefer, Deanna</creatorcontrib><creatorcontrib>Falkenberg, Lauren G.</creatorcontrib><creatorcontrib>Sullivan, Laura</creatorcontrib><creatorcontrib>Jaroncyk, Laura</creatorcontrib><creatorcontrib>Yang, Xiaojuan</creatorcontrib><creatorcontrib>Fisk, Harold</creatorcontrib><creatorcontrib>Wu, Lai-Chu</creatorcontrib><creatorcontrib>Hickey, Christopher</creatorcontrib><creatorcontrib>Chandler, Jason C.</creatorcontrib><creatorcontrib>Wu, Yue-Zhong</creatorcontrib><creatorcontrib>Heerema, Nyla A.</creatorcontrib><creatorcontrib>Chan, Kenneth K.</creatorcontrib><creatorcontrib>Perrotti, Danilo</creatorcontrib><creatorcontrib>Zhang, Jianying</creatorcontrib><creatorcontrib>Porcu, Pierluigi</creatorcontrib><creatorcontrib>Racke, Frederick K.</creatorcontrib><creatorcontrib>Garzon, Ramiro</creatorcontrib><creatorcontrib>Lee, Robert J.</creatorcontrib><creatorcontrib>Marcucci, Guido</creatorcontrib><creatorcontrib>Caligiuri, Michael A.</creatorcontrib><title>Aberrant Overexpression of IL-15 Initiates Large Granular Lymphocyte Leukemia through Chromosomal Instability and DNA Hypermethylation</title><title>Cancer cell</title><addtitle>Cancer Cell</addtitle><description>How inflammation causes cancer is unclear. Interleukin-15 (IL-15) is a pro-inflammatory cytokine elevated in human large granular lymphocyte (LGL) leukemia. Mice overexpressing IL-15 develop LGL leukemia. Here, we show that prolonged in vitro exposure of wild-type (WT) LGL to IL-15 results in Myc-mediated upregulation of aurora kinases, centrosome aberrancies, and aneuploidy. Simultaneously, IL-15 represses miR-29b via induction of Myc/NF-κBp65/Hdac-1, resulting in Dnmt3b overexpression and DNA hypermethylation. All this is validated in human LGL leukemia. Adoptive transfer of WT LGL cultured with IL-15 led to malignant transformation in vivo. Drug targeting that reverses miR-29b repression cures otherwise fatal LGL leukemia. We show how excessive IL-15 initiates cancer and demonstrate effective drug targeting for potential therapy of human LGL leukemia.
► A single pro-inflammatory cytokine, IL-15, can initiate malignant transformation ► IL-15-mediated induction of Myc is central to the genesis of leukemia ► Targeting miR-29b with a single therapeutic induces long-term remission of leukemia</description><subject>Aneuploidy</subject><subject>Animals</subject><subject>Cell Transformation, Neoplastic - genetics</subject><subject>Centrosome - physiology</subject><subject>Chromosomal Instability</subject><subject>Chromosome Segregation</subject><subject>DNA (Cytosine-5-)-Methyltransferases - genetics</subject><subject>DNA (Cytosine-5-)-Methyltransferases - metabolism</subject><subject>DNA Methylation</subject><subject>DNA Methyltransferase 3B</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Humans</subject><subject>Interleukin-15 - genetics</subject><subject>Interleukin-15 - metabolism</subject><subject>Leukemia, Large Granular Lymphocytic - genetics</subject><subject>Leukemia, Large Granular Lymphocytic - metabolism</subject><subject>Mice</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - metabolism</subject><issn>1535-6108</issn><issn>1878-3686</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kd1q3DAQhUVpadK0D9Cbohewo5-VLVMoLNsmWTDJTXMtZHm81ta2jKRd4hfoc1fLpqG9ycUwA3PONwwHoc-U5JTQ4nqfG-NzRijLSZUTUr1Bl1SWMuOFLN6mWXCRFZTIC_QhhD1JHlpW79EF46cVLy_R73UD3usp4ocjeHiaPYRg3YRdh7d1RgXeTjZaHSHgWvsd4NukPgza43oZ596ZJQKu4fALRqtx7L077Hq8SX10wY16SIAQdWMHGxespxZ_v1_ju2UGP0Lsl0HHdO4jetfpIcCn536FHm9-_NzcZfXD7XazrjMjaBmzjlZMrJhgZcsl0UwzXjSiWlVSSN4R01Ii-IoRAGgaKiSsWioKUxBRtZIk0xX6dubOh2aE1sAUvR7U7O2o_aKctur_zWR7tXNHxQtWpkoAegYY70Lw0L14KVGnUNRepVDUKRRFKpVCSZ4v_x59cfxNIQm-ngWQXj9a8CoYC5OB1nowUbXOvoL_Aze5n-Q</recordid><startdate>20121113</startdate><enddate>20121113</enddate><creator>Mishra, Anjali</creator><creator>Liu, Shujun</creator><creator>Sams, Gregory H.</creator><creator>Curphey, Douglas P.</creator><creator>Santhanam, Ramasamy</creator><creator>Rush, Laura J.</creator><creator>Schaefer, Deanna</creator><creator>Falkenberg, Lauren G.</creator><creator>Sullivan, Laura</creator><creator>Jaroncyk, Laura</creator><creator>Yang, Xiaojuan</creator><creator>Fisk, Harold</creator><creator>Wu, Lai-Chu</creator><creator>Hickey, Christopher</creator><creator>Chandler, Jason C.</creator><creator>Wu, Yue-Zhong</creator><creator>Heerema, Nyla A.</creator><creator>Chan, Kenneth K.</creator><creator>Perrotti, Danilo</creator><creator>Zhang, Jianying</creator><creator>Porcu, Pierluigi</creator><creator>Racke, Frederick K.</creator><creator>Garzon, Ramiro</creator><creator>Lee, Robert J.</creator><creator>Marcucci, Guido</creator><creator>Caligiuri, Michael A.</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</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>5PM</scope></search><sort><creationdate>20121113</creationdate><title>Aberrant Overexpression of IL-15 Initiates Large Granular Lymphocyte Leukemia through Chromosomal Instability and DNA Hypermethylation</title><author>Mishra, Anjali ; Liu, Shujun ; Sams, Gregory H. ; Curphey, Douglas P. ; Santhanam, Ramasamy ; Rush, Laura J. ; Schaefer, Deanna ; Falkenberg, Lauren G. ; Sullivan, Laura ; Jaroncyk, Laura ; Yang, Xiaojuan ; Fisk, Harold ; Wu, Lai-Chu ; Hickey, Christopher ; Chandler, Jason C. ; Wu, Yue-Zhong ; Heerema, Nyla A. ; Chan, Kenneth K. ; Perrotti, Danilo ; Zhang, Jianying ; Porcu, Pierluigi ; Racke, Frederick K. ; Garzon, Ramiro ; Lee, Robert J. ; Marcucci, Guido ; Caligiuri, Michael A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c517t-f192542527d380a2a236b59498583f0cd1053420eeebb158e4d156c6059d807d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Aneuploidy</topic><topic>Animals</topic><topic>Cell Transformation, Neoplastic - genetics</topic><topic>Centrosome - physiology</topic><topic>Chromosomal Instability</topic><topic>Chromosome Segregation</topic><topic>DNA (Cytosine-5-)-Methyltransferases - genetics</topic><topic>DNA (Cytosine-5-)-Methyltransferases - metabolism</topic><topic>DNA Methylation</topic><topic>DNA Methyltransferase 3B</topic><topic>Gene Expression Regulation, Neoplastic</topic><topic>Humans</topic><topic>Interleukin-15 - genetics</topic><topic>Interleukin-15 - metabolism</topic><topic>Leukemia, Large Granular Lymphocytic - genetics</topic><topic>Leukemia, Large Granular Lymphocytic - metabolism</topic><topic>Mice</topic><topic>MicroRNAs - genetics</topic><topic>MicroRNAs - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mishra, Anjali</creatorcontrib><creatorcontrib>Liu, Shujun</creatorcontrib><creatorcontrib>Sams, Gregory H.</creatorcontrib><creatorcontrib>Curphey, Douglas P.</creatorcontrib><creatorcontrib>Santhanam, Ramasamy</creatorcontrib><creatorcontrib>Rush, Laura J.</creatorcontrib><creatorcontrib>Schaefer, Deanna</creatorcontrib><creatorcontrib>Falkenberg, Lauren G.</creatorcontrib><creatorcontrib>Sullivan, Laura</creatorcontrib><creatorcontrib>Jaroncyk, Laura</creatorcontrib><creatorcontrib>Yang, Xiaojuan</creatorcontrib><creatorcontrib>Fisk, Harold</creatorcontrib><creatorcontrib>Wu, Lai-Chu</creatorcontrib><creatorcontrib>Hickey, Christopher</creatorcontrib><creatorcontrib>Chandler, Jason C.</creatorcontrib><creatorcontrib>Wu, Yue-Zhong</creatorcontrib><creatorcontrib>Heerema, Nyla A.</creatorcontrib><creatorcontrib>Chan, Kenneth K.</creatorcontrib><creatorcontrib>Perrotti, Danilo</creatorcontrib><creatorcontrib>Zhang, Jianying</creatorcontrib><creatorcontrib>Porcu, Pierluigi</creatorcontrib><creatorcontrib>Racke, Frederick K.</creatorcontrib><creatorcontrib>Garzon, Ramiro</creatorcontrib><creatorcontrib>Lee, Robert J.</creatorcontrib><creatorcontrib>Marcucci, Guido</creatorcontrib><creatorcontrib>Caligiuri, Michael A.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Cancer cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mishra, Anjali</au><au>Liu, Shujun</au><au>Sams, Gregory H.</au><au>Curphey, Douglas P.</au><au>Santhanam, Ramasamy</au><au>Rush, Laura J.</au><au>Schaefer, Deanna</au><au>Falkenberg, Lauren G.</au><au>Sullivan, Laura</au><au>Jaroncyk, Laura</au><au>Yang, Xiaojuan</au><au>Fisk, Harold</au><au>Wu, Lai-Chu</au><au>Hickey, Christopher</au><au>Chandler, Jason C.</au><au>Wu, Yue-Zhong</au><au>Heerema, Nyla A.</au><au>Chan, Kenneth K.</au><au>Perrotti, Danilo</au><au>Zhang, Jianying</au><au>Porcu, Pierluigi</au><au>Racke, Frederick K.</au><au>Garzon, Ramiro</au><au>Lee, Robert J.</au><au>Marcucci, Guido</au><au>Caligiuri, Michael A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Aberrant Overexpression of IL-15 Initiates Large Granular Lymphocyte Leukemia through Chromosomal Instability and DNA Hypermethylation</atitle><jtitle>Cancer cell</jtitle><addtitle>Cancer Cell</addtitle><date>2012-11-13</date><risdate>2012</risdate><volume>22</volume><issue>5</issue><spage>645</spage><epage>655</epage><pages>645-655</pages><issn>1535-6108</issn><eissn>1878-3686</eissn><abstract>How inflammation causes cancer is unclear. Interleukin-15 (IL-15) is a pro-inflammatory cytokine elevated in human large granular lymphocyte (LGL) leukemia. Mice overexpressing IL-15 develop LGL leukemia. Here, we show that prolonged in vitro exposure of wild-type (WT) LGL to IL-15 results in Myc-mediated upregulation of aurora kinases, centrosome aberrancies, and aneuploidy. Simultaneously, IL-15 represses miR-29b via induction of Myc/NF-κBp65/Hdac-1, resulting in Dnmt3b overexpression and DNA hypermethylation. All this is validated in human LGL leukemia. Adoptive transfer of WT LGL cultured with IL-15 led to malignant transformation in vivo. Drug targeting that reverses miR-29b repression cures otherwise fatal LGL leukemia. We show how excessive IL-15 initiates cancer and demonstrate effective drug targeting for potential therapy of human LGL leukemia.
► A single pro-inflammatory cytokine, IL-15, can initiate malignant transformation ► IL-15-mediated induction of Myc is central to the genesis of leukemia ► Targeting miR-29b with a single therapeutic induces long-term remission of leukemia</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>23153537</pmid><doi>10.1016/j.ccr.2012.09.009</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Cell Press Free Archives; Elsevier ScienceDirect Journals; EZB-FREE-00999 freely available EZB journals |
| subjects | Aneuploidy Animals Cell Transformation, Neoplastic - genetics Centrosome - physiology Chromosomal Instability Chromosome Segregation DNA (Cytosine-5-)-Methyltransferases - genetics DNA (Cytosine-5-)-Methyltransferases - metabolism DNA Methylation DNA Methyltransferase 3B Gene Expression Regulation, Neoplastic Humans Interleukin-15 - genetics Interleukin-15 - metabolism Leukemia, Large Granular Lymphocytic - genetics Leukemia, Large Granular Lymphocytic - metabolism Mice MicroRNAs - genetics MicroRNAs - metabolism |
| title | Aberrant Overexpression of IL-15 Initiates Large Granular Lymphocyte Leukemia through Chromosomal Instability and DNA Hypermethylation |
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