Virus-Tumor Interactome Screen Reveals ER Stress Response Can Reprogram Resistant Cancers for Oncolytic Virus-Triggered Caspase-2 Cell Death
To identify therapeutic opportunities for oncolytic viral therapy, we conducted genome-wide RNAi screens to search for host factors that modulate rhabdoviral oncolysis. Our screens uncovered the endoplasmic reticulum (ER) stress response pathways as important modulators of rhabdovirus-mediated cytot...
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| Veröffentlicht in: | Cancer cell 2011-10, Vol.20 (4), p.443-456 |
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| creator | Mahoney, Douglas J. Lefebvre, Charles Allan, Kristina Brun, Jan Sanaei, Cina A. Baird, Stephen Pearce, Nelson Grönberg, Susanna Wilson, Brian Prakesh, Mikael Aman, Ahmed Isaac, Methvin Mamai, Ahmed Uehling, David Al-Awar, Rima Falls, Theresa Alain, Tommy Stojdl, David F. |
| description | To identify therapeutic opportunities for oncolytic viral therapy, we conducted genome-wide RNAi screens to search for host factors that modulate rhabdoviral oncolysis. Our screens uncovered the endoplasmic reticulum (ER) stress response pathways as important modulators of rhabdovirus-mediated cytotoxicity. Further investigation revealed an unconventional mechanism whereby ER stress response inhibition preconditioned cancer cells, which sensitized them to caspase-2-dependent apoptosis induced by a subsequent rhabdovirus infection. Importantly, this mechanism was tumor cell specific, selectively increasing potency of the oncolytic virus by up to 10,000-fold. In vivo studies using a small molecule inhibitor of IRE1α showed dramatically improved oncolytic efficacy in resistant tumor models. Our study demonstrates proof of concept for using functional genomics to improve biotherapeutic agents for cancer.
► RNAi screen finds UPR/ERAD blockade sensitizes cancer cells to oncolytic therapy ► Cellular response to ER stress, not acute stress, predisposes cancer cells to death ► PIDD-independent caspase-2 mechanism is triggered by virus infection ► Chemical inhibition of IRE1α improves oncolytic virus therapy in vivo |
| doi_str_mv | 10.1016/j.ccr.2011.09.005 |
| format | Article |
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► RNAi screen finds UPR/ERAD blockade sensitizes cancer cells to oncolytic therapy ► Cellular response to ER stress, not acute stress, predisposes cancer cells to death ► PIDD-independent caspase-2 mechanism is triggered by virus infection ► Chemical inhibition of IRE1α improves oncolytic virus therapy in vivo</description><identifier>ISSN: 1535-6108</identifier><identifier>EISSN: 1878-3686</identifier><identifier>DOI: 10.1016/j.ccr.2011.09.005</identifier><identifier>PMID: 22014571</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Apoptosis - physiology ; Caspase 2 - metabolism ; Caspase 2 - physiology ; Cell Line, Tumor ; Cysteine Endopeptidases - metabolism ; Cysteine Endopeptidases - physiology ; Endoplasmic Reticulum - physiology ; Endoplasmic Reticulum Stress ; Endoribonucleases - antagonists & inhibitors ; Female ; Genomics - methods ; Glioblastoma - drug therapy ; Glioblastoma - pathology ; Glioblastoma - virology ; Humans ; Mice ; Mice, Nude ; Oncolytic Virotherapy - methods ; Oncolytic Viruses - immunology ; Oncolytic Viruses - metabolism ; Oncolytic Viruses - physiology ; Ovarian Neoplasms - drug therapy ; Ovarian Neoplasms - pathology ; Ovarian Neoplasms - virology ; Protein-Serine-Threonine Kinases - antagonists & inhibitors ; Rhabdoviridae - physiology ; Rhabdovirus ; RNA Interference</subject><ispartof>Cancer cell, 2011-10, Vol.20 (4), p.443-456</ispartof><rights>2011 Elsevier Inc.</rights><rights>Copyright © 2011 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c493t-aabb142854804cdf02f83fa38aa5bb3540b7f20194011171e798df4f9c611c423</citedby><cites>FETCH-LOGICAL-c493t-aabb142854804cdf02f83fa38aa5bb3540b7f20194011171e798df4f9c611c423</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1535610811003539$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22014571$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mahoney, Douglas J.</creatorcontrib><creatorcontrib>Lefebvre, Charles</creatorcontrib><creatorcontrib>Allan, Kristina</creatorcontrib><creatorcontrib>Brun, Jan</creatorcontrib><creatorcontrib>Sanaei, Cina A.</creatorcontrib><creatorcontrib>Baird, Stephen</creatorcontrib><creatorcontrib>Pearce, Nelson</creatorcontrib><creatorcontrib>Grönberg, Susanna</creatorcontrib><creatorcontrib>Wilson, Brian</creatorcontrib><creatorcontrib>Prakesh, Mikael</creatorcontrib><creatorcontrib>Aman, Ahmed</creatorcontrib><creatorcontrib>Isaac, Methvin</creatorcontrib><creatorcontrib>Mamai, Ahmed</creatorcontrib><creatorcontrib>Uehling, David</creatorcontrib><creatorcontrib>Al-Awar, Rima</creatorcontrib><creatorcontrib>Falls, Theresa</creatorcontrib><creatorcontrib>Alain, Tommy</creatorcontrib><creatorcontrib>Stojdl, David F.</creatorcontrib><title>Virus-Tumor Interactome Screen Reveals ER Stress Response Can Reprogram Resistant Cancers for Oncolytic Virus-Triggered Caspase-2 Cell Death</title><title>Cancer cell</title><addtitle>Cancer Cell</addtitle><description>To identify therapeutic opportunities for oncolytic viral therapy, we conducted genome-wide RNAi screens to search for host factors that modulate rhabdoviral oncolysis. Our screens uncovered the endoplasmic reticulum (ER) stress response pathways as important modulators of rhabdovirus-mediated cytotoxicity. Further investigation revealed an unconventional mechanism whereby ER stress response inhibition preconditioned cancer cells, which sensitized them to caspase-2-dependent apoptosis induced by a subsequent rhabdovirus infection. Importantly, this mechanism was tumor cell specific, selectively increasing potency of the oncolytic virus by up to 10,000-fold. In vivo studies using a small molecule inhibitor of IRE1α showed dramatically improved oncolytic efficacy in resistant tumor models. Our study demonstrates proof of concept for using functional genomics to improve biotherapeutic agents for cancer.
► RNAi screen finds UPR/ERAD blockade sensitizes cancer cells to oncolytic therapy ► Cellular response to ER stress, not acute stress, predisposes cancer cells to death ► PIDD-independent caspase-2 mechanism is triggered by virus infection ► Chemical inhibition of IRE1α improves oncolytic virus therapy in vivo</description><subject>Animals</subject><subject>Apoptosis - physiology</subject><subject>Caspase 2 - metabolism</subject><subject>Caspase 2 - physiology</subject><subject>Cell Line, Tumor</subject><subject>Cysteine Endopeptidases - metabolism</subject><subject>Cysteine Endopeptidases - physiology</subject><subject>Endoplasmic Reticulum - physiology</subject><subject>Endoplasmic Reticulum Stress</subject><subject>Endoribonucleases - antagonists & inhibitors</subject><subject>Female</subject><subject>Genomics - methods</subject><subject>Glioblastoma - drug therapy</subject><subject>Glioblastoma - pathology</subject><subject>Glioblastoma - virology</subject><subject>Humans</subject><subject>Mice</subject><subject>Mice, Nude</subject><subject>Oncolytic Virotherapy - methods</subject><subject>Oncolytic Viruses - immunology</subject><subject>Oncolytic Viruses - metabolism</subject><subject>Oncolytic Viruses - physiology</subject><subject>Ovarian Neoplasms - drug therapy</subject><subject>Ovarian Neoplasms - pathology</subject><subject>Ovarian Neoplasms - virology</subject><subject>Protein-Serine-Threonine Kinases - antagonists & inhibitors</subject><subject>Rhabdoviridae - physiology</subject><subject>Rhabdovirus</subject><subject>RNA Interference</subject><issn>1535-6108</issn><issn>1878-3686</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFUcFu1DAUtBCIlsIHcEG-cUp4TpzEFie0LVCpUqW2cLUc53nxapMstlOp_8BH86JdOMLJ1nhm3vMMY28FlAJE-2FXOhfLCoQoQZcAzTN2LlSnirpV7XO6N3VTtALUGXuV0g5IIzr9kp1VpJFNJ87Zr-8hLql4WMY58uspY7QuzyPyexcRJ36Hj2j3iV_d8fscMSVC0mGeEvKNXZ8Pcd5GO65wSNlOecUdxsQ9Od5Obt4_5eD4aU4M2y1GHIiVDjZhUfEN7vf8Em3-8Zq98DQM35zOC_bt89XD5mtxc_vlevPppnBS17mwtu-FrFQjFUg3eKi8qr2tlbVN39eNhL7z9EMtKRnRCey0Grz02rVCOFnVF-z90ZeW_7lgymYMydEadsJ5SUZX0GkNWvyfCdDW0HYNMcWR6eKcUkRvDjGMNj4ZAWZty-wMtWXWtgxoQ22R5t3JfelHHP4q_tRDhI9HAlIajwGjSS4gxTuEiC6bYQ7_sP8Nm1ilgg</recordid><startdate>20111018</startdate><enddate>20111018</enddate><creator>Mahoney, Douglas J.</creator><creator>Lefebvre, Charles</creator><creator>Allan, Kristina</creator><creator>Brun, Jan</creator><creator>Sanaei, Cina A.</creator><creator>Baird, Stephen</creator><creator>Pearce, Nelson</creator><creator>Grönberg, Susanna</creator><creator>Wilson, Brian</creator><creator>Prakesh, Mikael</creator><creator>Aman, Ahmed</creator><creator>Isaac, Methvin</creator><creator>Mamai, Ahmed</creator><creator>Uehling, David</creator><creator>Al-Awar, Rima</creator><creator>Falls, Theresa</creator><creator>Alain, Tommy</creator><creator>Stojdl, David F.</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>7X8</scope><scope>7TO</scope><scope>7U9</scope><scope>H94</scope></search><sort><creationdate>20111018</creationdate><title>Virus-Tumor Interactome Screen Reveals ER Stress Response Can Reprogram Resistant Cancers for Oncolytic Virus-Triggered Caspase-2 Cell Death</title><author>Mahoney, Douglas J. ; Lefebvre, Charles ; Allan, Kristina ; Brun, Jan ; Sanaei, Cina A. ; Baird, Stephen ; Pearce, Nelson ; Grönberg, Susanna ; Wilson, Brian ; Prakesh, Mikael ; Aman, Ahmed ; Isaac, Methvin ; Mamai, Ahmed ; Uehling, David ; Al-Awar, Rima ; Falls, Theresa ; Alain, Tommy ; Stojdl, David F.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c493t-aabb142854804cdf02f83fa38aa5bb3540b7f20194011171e798df4f9c611c423</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Animals</topic><topic>Apoptosis - physiology</topic><topic>Caspase 2 - metabolism</topic><topic>Caspase 2 - physiology</topic><topic>Cell Line, Tumor</topic><topic>Cysteine Endopeptidases - metabolism</topic><topic>Cysteine Endopeptidases - physiology</topic><topic>Endoplasmic Reticulum - physiology</topic><topic>Endoplasmic Reticulum Stress</topic><topic>Endoribonucleases - antagonists & inhibitors</topic><topic>Female</topic><topic>Genomics - methods</topic><topic>Glioblastoma - drug therapy</topic><topic>Glioblastoma - pathology</topic><topic>Glioblastoma - virology</topic><topic>Humans</topic><topic>Mice</topic><topic>Mice, Nude</topic><topic>Oncolytic Virotherapy - methods</topic><topic>Oncolytic Viruses - immunology</topic><topic>Oncolytic Viruses - metabolism</topic><topic>Oncolytic Viruses - physiology</topic><topic>Ovarian Neoplasms - drug therapy</topic><topic>Ovarian Neoplasms - pathology</topic><topic>Ovarian Neoplasms - virology</topic><topic>Protein-Serine-Threonine Kinases - antagonists & inhibitors</topic><topic>Rhabdoviridae - physiology</topic><topic>Rhabdovirus</topic><topic>RNA Interference</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mahoney, Douglas J.</creatorcontrib><creatorcontrib>Lefebvre, Charles</creatorcontrib><creatorcontrib>Allan, Kristina</creatorcontrib><creatorcontrib>Brun, Jan</creatorcontrib><creatorcontrib>Sanaei, Cina A.</creatorcontrib><creatorcontrib>Baird, Stephen</creatorcontrib><creatorcontrib>Pearce, Nelson</creatorcontrib><creatorcontrib>Grönberg, Susanna</creatorcontrib><creatorcontrib>Wilson, Brian</creatorcontrib><creatorcontrib>Prakesh, Mikael</creatorcontrib><creatorcontrib>Aman, Ahmed</creatorcontrib><creatorcontrib>Isaac, Methvin</creatorcontrib><creatorcontrib>Mamai, Ahmed</creatorcontrib><creatorcontrib>Uehling, David</creatorcontrib><creatorcontrib>Al-Awar, Rima</creatorcontrib><creatorcontrib>Falls, Theresa</creatorcontrib><creatorcontrib>Alain, Tommy</creatorcontrib><creatorcontrib>Stojdl, David F.</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>MEDLINE - Academic</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><jtitle>Cancer cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mahoney, Douglas J.</au><au>Lefebvre, Charles</au><au>Allan, Kristina</au><au>Brun, Jan</au><au>Sanaei, Cina A.</au><au>Baird, Stephen</au><au>Pearce, Nelson</au><au>Grönberg, Susanna</au><au>Wilson, Brian</au><au>Prakesh, Mikael</au><au>Aman, Ahmed</au><au>Isaac, Methvin</au><au>Mamai, Ahmed</au><au>Uehling, David</au><au>Al-Awar, Rima</au><au>Falls, Theresa</au><au>Alain, Tommy</au><au>Stojdl, David F.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Virus-Tumor Interactome Screen Reveals ER Stress Response Can Reprogram Resistant Cancers for Oncolytic Virus-Triggered Caspase-2 Cell Death</atitle><jtitle>Cancer cell</jtitle><addtitle>Cancer Cell</addtitle><date>2011-10-18</date><risdate>2011</risdate><volume>20</volume><issue>4</issue><spage>443</spage><epage>456</epage><pages>443-456</pages><issn>1535-6108</issn><eissn>1878-3686</eissn><abstract>To identify therapeutic opportunities for oncolytic viral therapy, we conducted genome-wide RNAi screens to search for host factors that modulate rhabdoviral oncolysis. Our screens uncovered the endoplasmic reticulum (ER) stress response pathways as important modulators of rhabdovirus-mediated cytotoxicity. Further investigation revealed an unconventional mechanism whereby ER stress response inhibition preconditioned cancer cells, which sensitized them to caspase-2-dependent apoptosis induced by a subsequent rhabdovirus infection. Importantly, this mechanism was tumor cell specific, selectively increasing potency of the oncolytic virus by up to 10,000-fold. In vivo studies using a small molecule inhibitor of IRE1α showed dramatically improved oncolytic efficacy in resistant tumor models. Our study demonstrates proof of concept for using functional genomics to improve biotherapeutic agents for cancer.
► RNAi screen finds UPR/ERAD blockade sensitizes cancer cells to oncolytic therapy ► Cellular response to ER stress, not acute stress, predisposes cancer cells to death ► PIDD-independent caspase-2 mechanism is triggered by virus infection ► Chemical inhibition of IRE1α improves oncolytic virus therapy in vivo</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>22014571</pmid><doi>10.1016/j.ccr.2011.09.005</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Apoptosis - physiology Caspase 2 - metabolism Caspase 2 - physiology Cell Line, Tumor Cysteine Endopeptidases - metabolism Cysteine Endopeptidases - physiology Endoplasmic Reticulum - physiology Endoplasmic Reticulum Stress Endoribonucleases - antagonists & inhibitors Female Genomics - methods Glioblastoma - drug therapy Glioblastoma - pathology Glioblastoma - virology Humans Mice Mice, Nude Oncolytic Virotherapy - methods Oncolytic Viruses - immunology Oncolytic Viruses - metabolism Oncolytic Viruses - physiology Ovarian Neoplasms - drug therapy Ovarian Neoplasms - pathology Ovarian Neoplasms - virology Protein-Serine-Threonine Kinases - antagonists & inhibitors Rhabdoviridae - physiology Rhabdovirus RNA Interference |
| title | Virus-Tumor Interactome Screen Reveals ER Stress Response Can Reprogram Resistant Cancers for Oncolytic Virus-Triggered Caspase-2 Cell Death |
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