PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis
Cancer cells can divert metabolites into anabolic pathways to support their rapid proliferation and to accumulate the cellular building blocks required for tumour growth. However, the specific bioenergetic profile of invasive and metastatic cancer cells is unknown. Here we report that migratory/inva...
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| Veröffentlicht in: | Nature cell biology 2014-10, Vol.16 (10), p.992-1003 |
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| creator | LeBleu, Valerie S. O’Connell, Joyce T. Gonzalez Herrera, Karina N. Wikman, Harriet Pantel, Klaus Haigis, Marcia C. de Carvalho, Fernanda Machado Damascena, Aline Domingos Chinen, Ludmilla Thome Rocha, Rafael M. Asara, John M. Kalluri, Raghu |
| description | Cancer cells can divert metabolites into anabolic pathways to support their rapid proliferation and to accumulate the cellular building blocks required for tumour growth. However, the specific bioenergetic profile of invasive and metastatic cancer cells is unknown. Here we report that migratory/invasive cancer cells specifically favour mitochondrial respiration and increased ATP production. Invasive cancer cells use the transcription coactivator peroxisome proliferator-activated receptor gamma, coactivator 1 alpha (PPARGC1A, also known as PGC-1α) to enhance oxidative phosphorylation, mitochondrial biogenesis and the oxygen consumption rate. Clinical analysis of human invasive breast cancers revealed a strong correlation between PGC-1α expression in invasive cancer cells and the formation of distant metastases. Silencing of PGC-1α in cancer cells suspended their invasive potential and attenuated metastasis without affecting proliferation, primary tumour growth or the epithelial-to-mesenchymal program. Inherent genetics of cancer cells can determine the transcriptome framework associated with invasion and metastasis, and mitochondrial biogenesis and respiration induced by PGC-1α are also essential for functional motility of cancer cells and metastasis.
Kalluri and colleagues find that mitochondrial biogenesis and respiration induced by transcriptional coactivator PGC-1α in cancer cells promote cancer metastasis and that PGC-1α expression is associated with invasive breast cancer. |
| doi_str_mv | 10.1038/ncb3039 |
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Kalluri and colleagues find that mitochondrial biogenesis and respiration induced by transcriptional coactivator PGC-1α in cancer cells promote cancer metastasis and that PGC-1α expression is associated with invasive breast cancer.</description><identifier>ISSN: 1465-7392</identifier><identifier>EISSN: 1476-4679</identifier><identifier>DOI: 10.1038/ncb3039</identifier><identifier>PMID: 25241037</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>49/39 ; 49/88 ; 631/1647/2017 ; 631/67/2327 ; 631/67/322 ; 64/60 ; 82/51 ; 96/106 ; Animals ; Blotting, Western ; Breast Neoplasms - genetics ; Breast Neoplasms - metabolism ; Breast Neoplasms - pathology ; Cancer cells ; Cancer Research ; Cell Biology ; Cell Line, Tumor ; Cell Movement ; Development and progression ; Developmental Biology ; Female ; Gene Expression Profiling ; Gene Expression Regulation, Neoplastic ; Genetic aspects ; Humans ; Immunohistochemistry ; Life Sciences ; Male ; Metastasis ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Nude ; Microscopy, Electron, Transmission ; Middle Aged ; Mitochondria ; Mitochondria - metabolism ; Neoplasm Invasiveness ; Neoplasm Metastasis ; Neoplasms - genetics ; Neoplasms - metabolism ; Neoplasms - ultrastructure ; Oxidative Phosphorylation ; Oxygen Consumption ; Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha ; Properties ; Reverse Transcriptase Polymerase Chain Reaction ; RNA Interference ; Stem Cells ; Transcription factors ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>Nature cell biology, 2014-10, Vol.16 (10), p.992-1003</ispartof><rights>Springer Nature Limited 2014</rights><rights>COPYRIGHT 2014 Nature Publishing Group</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5029-f41d5c2c3671eec7cd4eb3c48388096263daac21b80ca41d825258dc7174e7643</citedby><cites>FETCH-LOGICAL-c5029-f41d5c2c3671eec7cd4eb3c48388096263daac21b80ca41d825258dc7174e7643</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/ncb3039$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/ncb3039$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25241037$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>LeBleu, Valerie S.</creatorcontrib><creatorcontrib>O’Connell, Joyce T.</creatorcontrib><creatorcontrib>Gonzalez Herrera, Karina N.</creatorcontrib><creatorcontrib>Wikman, Harriet</creatorcontrib><creatorcontrib>Pantel, Klaus</creatorcontrib><creatorcontrib>Haigis, Marcia C.</creatorcontrib><creatorcontrib>de Carvalho, Fernanda Machado</creatorcontrib><creatorcontrib>Damascena, Aline</creatorcontrib><creatorcontrib>Domingos Chinen, Ludmilla Thome</creatorcontrib><creatorcontrib>Rocha, Rafael M.</creatorcontrib><creatorcontrib>Asara, John M.</creatorcontrib><creatorcontrib>Kalluri, Raghu</creatorcontrib><title>PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis</title><title>Nature cell biology</title><addtitle>Nat Cell Biol</addtitle><addtitle>Nat Cell Biol</addtitle><description>Cancer cells can divert metabolites into anabolic pathways to support their rapid proliferation and to accumulate the cellular building blocks required for tumour growth. However, the specific bioenergetic profile of invasive and metastatic cancer cells is unknown. Here we report that migratory/invasive cancer cells specifically favour mitochondrial respiration and increased ATP production. Invasive cancer cells use the transcription coactivator peroxisome proliferator-activated receptor gamma, coactivator 1 alpha (PPARGC1A, also known as PGC-1α) to enhance oxidative phosphorylation, mitochondrial biogenesis and the oxygen consumption rate. Clinical analysis of human invasive breast cancers revealed a strong correlation between PGC-1α expression in invasive cancer cells and the formation of distant metastases. Silencing of PGC-1α in cancer cells suspended their invasive potential and attenuated metastasis without affecting proliferation, primary tumour growth or the epithelial-to-mesenchymal program. Inherent genetics of cancer cells can determine the transcriptome framework associated with invasion and metastasis, and mitochondrial biogenesis and respiration induced by PGC-1α are also essential for functional motility of cancer cells and metastasis.
Kalluri and colleagues find that mitochondrial biogenesis and respiration induced by transcriptional coactivator PGC-1α in cancer cells promote cancer metastasis and that PGC-1α expression is associated with invasive breast cancer.</description><subject>49/39</subject><subject>49/88</subject><subject>631/1647/2017</subject><subject>631/67/2327</subject><subject>631/67/322</subject><subject>64/60</subject><subject>82/51</subject><subject>96/106</subject><subject>Animals</subject><subject>Blotting, Western</subject><subject>Breast Neoplasms - genetics</subject><subject>Breast Neoplasms - metabolism</subject><subject>Breast Neoplasms - pathology</subject><subject>Cancer cells</subject><subject>Cancer Research</subject><subject>Cell Biology</subject><subject>Cell Line, Tumor</subject><subject>Cell Movement</subject><subject>Development and progression</subject><subject>Developmental Biology</subject><subject>Female</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Genetic aspects</subject><subject>Humans</subject><subject>Immunohistochemistry</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Metastasis</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Nude</subject><subject>Microscopy, Electron, Transmission</subject><subject>Middle Aged</subject><subject>Mitochondria</subject><subject>Mitochondria - metabolism</subject><subject>Neoplasm Invasiveness</subject><subject>Neoplasm Metastasis</subject><subject>Neoplasms - genetics</subject><subject>Neoplasms - metabolism</subject><subject>Neoplasms - ultrastructure</subject><subject>Oxidative Phosphorylation</subject><subject>Oxygen Consumption</subject><subject>Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha</subject><subject>Properties</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>RNA Interference</subject><subject>Stem Cells</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><issn>1465-7392</issn><issn>1476-4679</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqVkl1uFSEYhidGY2s17sCQeKFeTIWBAeayObG1SRONP9eEgW9OaWbgCIxpd-MWugUX4Jpkco6aE72oAcLf8718wFtVTwk-JpjK1970FNPuXnVImOA146K7v4x5WwvaNQfVo5SuMCaMYfGwOmjahpU4cVj592ermvy4RRNYpzMkNLkczGXwNjo9ot6FNXhILiHtLQrXzursvgLaXIZUWrwZyzx45Dwy2huIyMA4JpQD2sQwhQzfv02QdSrVpcfVg0GPCZ7s-qPq8-mbT6u39cW7s_PVyUVtWtx09cCIbU1jKBcEwAhjGfTUMEmlxB1vOLVam4b0EhtdWFku1EprBBEMBGf0qHq51S05fJkhZTW5tCSmPYQ5KdJKTjAhHSno8y261iMo54eQozYLrk6obCWmuBF3onihjv9BlWJhciZ4GFxZ35P9r4DlhFd7AYXJcJ3Xek5JnX_8sC9-V3bRfbFlTQwpRRjUJrpJxxtFsFospnYWK-Sz3dPOfTHNb-6Xp_68fSpbfg1RXYU5-vLdf2n9BIhb1qc</recordid><startdate>20141001</startdate><enddate>20141001</enddate><creator>LeBleu, Valerie S.</creator><creator>O’Connell, Joyce T.</creator><creator>Gonzalez Herrera, Karina N.</creator><creator>Wikman, Harriet</creator><creator>Pantel, Klaus</creator><creator>Haigis, Marcia C.</creator><creator>de Carvalho, Fernanda Machado</creator><creator>Damascena, Aline</creator><creator>Domingos Chinen, Ludmilla Thome</creator><creator>Rocha, Rafael M.</creator><creator>Asara, John M.</creator><creator>Kalluri, Raghu</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><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>ISR</scope><scope>7X8</scope></search><sort><creationdate>20141001</creationdate><title>PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis</title><author>LeBleu, Valerie S. ; O’Connell, Joyce T. ; Gonzalez Herrera, Karina N. ; Wikman, Harriet ; Pantel, Klaus ; Haigis, Marcia C. ; de Carvalho, Fernanda Machado ; Damascena, Aline ; Domingos Chinen, Ludmilla Thome ; Rocha, Rafael M. ; Asara, John M. ; Kalluri, Raghu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5029-f41d5c2c3671eec7cd4eb3c48388096263daac21b80ca41d825258dc7174e7643</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>49/39</topic><topic>49/88</topic><topic>631/1647/2017</topic><topic>631/67/2327</topic><topic>631/67/322</topic><topic>64/60</topic><topic>82/51</topic><topic>96/106</topic><topic>Animals</topic><topic>Blotting, Western</topic><topic>Breast Neoplasms - genetics</topic><topic>Breast Neoplasms - metabolism</topic><topic>Breast Neoplasms - pathology</topic><topic>Cancer cells</topic><topic>Cancer Research</topic><topic>Cell Biology</topic><topic>Cell Line, Tumor</topic><topic>Cell Movement</topic><topic>Development and progression</topic><topic>Developmental Biology</topic><topic>Female</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Neoplastic</topic><topic>Genetic aspects</topic><topic>Humans</topic><topic>Immunohistochemistry</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Metastasis</topic><topic>Mice, Inbred BALB C</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Nude</topic><topic>Microscopy, Electron, Transmission</topic><topic>Middle Aged</topic><topic>Mitochondria</topic><topic>Mitochondria - metabolism</topic><topic>Neoplasm Invasiveness</topic><topic>Neoplasm Metastasis</topic><topic>Neoplasms - genetics</topic><topic>Neoplasms - metabolism</topic><topic>Neoplasms - ultrastructure</topic><topic>Oxidative Phosphorylation</topic><topic>Oxygen Consumption</topic><topic>Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha</topic><topic>Properties</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>RNA Interference</topic><topic>Stem Cells</topic><topic>Transcription factors</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>LeBleu, Valerie S.</creatorcontrib><creatorcontrib>O’Connell, Joyce T.</creatorcontrib><creatorcontrib>Gonzalez Herrera, Karina N.</creatorcontrib><creatorcontrib>Wikman, Harriet</creatorcontrib><creatorcontrib>Pantel, Klaus</creatorcontrib><creatorcontrib>Haigis, Marcia C.</creatorcontrib><creatorcontrib>de Carvalho, Fernanda Machado</creatorcontrib><creatorcontrib>Damascena, Aline</creatorcontrib><creatorcontrib>Domingos Chinen, Ludmilla Thome</creatorcontrib><creatorcontrib>Rocha, Rafael M.</creatorcontrib><creatorcontrib>Asara, John M.</creatorcontrib><creatorcontrib>Kalluri, Raghu</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><jtitle>Nature cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>LeBleu, Valerie S.</au><au>O’Connell, Joyce T.</au><au>Gonzalez Herrera, Karina N.</au><au>Wikman, Harriet</au><au>Pantel, Klaus</au><au>Haigis, Marcia C.</au><au>de Carvalho, Fernanda Machado</au><au>Damascena, Aline</au><au>Domingos Chinen, Ludmilla Thome</au><au>Rocha, Rafael M.</au><au>Asara, John M.</au><au>Kalluri, Raghu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis</atitle><jtitle>Nature cell biology</jtitle><stitle>Nat Cell Biol</stitle><addtitle>Nat Cell Biol</addtitle><date>2014-10-01</date><risdate>2014</risdate><volume>16</volume><issue>10</issue><spage>992</spage><epage>1003</epage><pages>992-1003</pages><issn>1465-7392</issn><eissn>1476-4679</eissn><abstract>Cancer cells can divert metabolites into anabolic pathways to support their rapid proliferation and to accumulate the cellular building blocks required for tumour growth. However, the specific bioenergetic profile of invasive and metastatic cancer cells is unknown. Here we report that migratory/invasive cancer cells specifically favour mitochondrial respiration and increased ATP production. Invasive cancer cells use the transcription coactivator peroxisome proliferator-activated receptor gamma, coactivator 1 alpha (PPARGC1A, also known as PGC-1α) to enhance oxidative phosphorylation, mitochondrial biogenesis and the oxygen consumption rate. Clinical analysis of human invasive breast cancers revealed a strong correlation between PGC-1α expression in invasive cancer cells and the formation of distant metastases. Silencing of PGC-1α in cancer cells suspended their invasive potential and attenuated metastasis without affecting proliferation, primary tumour growth or the epithelial-to-mesenchymal program. Inherent genetics of cancer cells can determine the transcriptome framework associated with invasion and metastasis, and mitochondrial biogenesis and respiration induced by PGC-1α are also essential for functional motility of cancer cells and metastasis.
Kalluri and colleagues find that mitochondrial biogenesis and respiration induced by transcriptional coactivator PGC-1α in cancer cells promote cancer metastasis and that PGC-1α expression is associated with invasive breast cancer.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>25241037</pmid><doi>10.1038/ncb3039</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 49/39 49/88 631/1647/2017 631/67/2327 631/67/322 64/60 82/51 96/106 Animals Blotting, Western Breast Neoplasms - genetics Breast Neoplasms - metabolism Breast Neoplasms - pathology Cancer cells Cancer Research Cell Biology Cell Line, Tumor Cell Movement Development and progression Developmental Biology Female Gene Expression Profiling Gene Expression Regulation, Neoplastic Genetic aspects Humans Immunohistochemistry Life Sciences Male Metastasis Mice, Inbred BALB C Mice, Inbred C57BL Mice, Nude Microscopy, Electron, Transmission Middle Aged Mitochondria Mitochondria - metabolism Neoplasm Invasiveness Neoplasm Metastasis Neoplasms - genetics Neoplasms - metabolism Neoplasms - ultrastructure Oxidative Phosphorylation Oxygen Consumption Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha Properties Reverse Transcriptase Polymerase Chain Reaction RNA Interference Stem Cells Transcription factors Transcription Factors - genetics Transcription Factors - metabolism |
| title | PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis |
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