Metabolic-Pathway-Based Subtyping of Triple-Negative Breast Cancer Reveals Potential Therapeutic Targets
Triple-negative breast cancer (TNBC) remains an unmet medical challenge. We investigated metabolic dysregulation in TNBCs by using our multi-omics database (n = 465, the largest to date). TNBC samples were classified into three heterogeneous metabolic-pathway-based subtypes (MPSs) with distinct meta...
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creator | Gong, Yue Ji, Peng Yang, Yun-Song Xie, Shao Yu, Tian-Jian Xiao, Yi Jin, Ming-Liang Ma, Ding Guo, Lin-Wei Pei, Yu-Chen Chai, Wen-Jun Li, Da-Qiang Bai, Fan Bertucci, François Hu, Xin Jiang, Yi-Zhou Shao, Zhi-Ming |
description | Triple-negative breast cancer (TNBC) remains an unmet medical challenge. We investigated metabolic dysregulation in TNBCs by using our multi-omics database (n = 465, the largest to date). TNBC samples were classified into three heterogeneous metabolic-pathway-based subtypes (MPSs) with distinct metabolic features: MPS1, the lipogenic subtype with upregulated lipid metabolism; MPS2, the glycolytic subtype with upregulated carbohydrate and nucleotide metabolism; and MPS3, the mixed subtype with partial pathway dysregulation. These subtypes were validated by metabolomic profiling of 72 samples. These three subtypes had distinct prognoses, molecular subtype distributions, and genomic alterations. Moreover, MPS1 TNBCs were more sensitive to metabolic inhibitors targeting fatty acid synthesis, whereas MPS2 TNBCs showed higher sensitivity to inhibitors targeting glycolysis. Importantly, inhibition of lactate dehydrogenase could enhance tumor response to anti-PD-1 immunotherapy in MPS2 TNBCs. Collectively, our analysis demonstrated the metabolic heterogeneity of TNBCs and enabled the development of personalized therapies targeting unique tumor metabolic profiles.
[Display omitted]
•The metabolic reprogramming and heterogeneity of TNBC is systematically characterized•TNBCs are classified into three subtypes on the basis of metabolic pathways•Three subtypes show distinct sensitivities to various metabolic inhibitors•Inhibition of LDH enhances tumor response to anti-PD-1 immunotherapy in MPS2 TNBCs
Gong et al. reveal the metabolic heterogeneity of triple-negative breast cancer and identify three metabolic-pathway-based subtypes with distinct molecular features and sensitivities to various metabolic inhibitors. They find that inhibition of lactate dehydrogenase could enhance the anti-PD-1 immunotherapy response in a certain subtype of triple-negative breast cancer. |
doi_str_mv | 10.1016/j.cmet.2020.10.012 |
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fullrecord | <record><control><sourceid>proquest_hal_p</sourceid><recordid>TN_cdi_hal_primary_oai_HAL_hal_03623115v1</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S1550413120305453</els_id><sourcerecordid>2460769843</sourcerecordid><originalsourceid>FETCH-LOGICAL-c483t-cdcf93ec5b460094f5bc8125ed0fca33286bb37c17b7431a87dd7558fbfc468f3</originalsourceid><addsrcrecordid>eNp9kUtv2zAQhIkiRfPqH8gh4DE9yOVDTyCXxGiaAm4TtO6ZWFJLm4ZsqSTlwv--FJzk2NMuBt8OFjOEXHE244yXnzczs8U4E0xMwoxx8Y6c8UaKrMoFO0l7UbAs55KfkvMQNozJUjbyAzmVktecNfyMrL9jBN13zmTPENd_4ZDdQ8CW_hp1PAxut6K9pUvvhg6zH7iC6PZI7z1CiHQOO4Oe_sQ9Qhfocx9xFx10dLlGDwOO0Rm6BL_CGC7Je5sg_PgyL8jvhy_L-WO2ePr6bX63yExey5iZ1thGoil0XjLW5LbQpuaiwJZZA1KKutRaVoZXusolh7pq26ooaqutycvaygvy6ei7hk4N3m3BH1QPTj3eLdSkpRCE5LzY88TeHNnB939GDFFtXTDYdbDDfgxKpB-qsqlzmVBxRI3vQ_Bo37w5U1MbaqOmNtTUxqSlNtLR9Yv_qLfYvp28xp-A2yOAKZG9Q6-CcZhCbZ1HE1Xbu__5_wMU3pt5</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2460769843</pqid></control><display><type>article</type><title>Metabolic-Pathway-Based Subtyping of Triple-Negative Breast Cancer Reveals Potential Therapeutic Targets</title><source>MEDLINE</source><source>Cell Press Free Archives</source><source>Access via ScienceDirect (Elsevier)</source><source>EZB-FREE-00999 freely available EZB journals</source><creator>Gong, Yue ; Ji, Peng ; Yang, Yun-Song ; Xie, Shao ; Yu, Tian-Jian ; Xiao, Yi ; Jin, Ming-Liang ; Ma, Ding ; Guo, Lin-Wei ; Pei, Yu-Chen ; Chai, Wen-Jun ; Li, Da-Qiang ; Bai, Fan ; Bertucci, François ; Hu, Xin ; Jiang, Yi-Zhou ; Shao, Zhi-Ming</creator><creatorcontrib>Gong, Yue ; Ji, Peng ; Yang, Yun-Song ; Xie, Shao ; Yu, Tian-Jian ; Xiao, Yi ; Jin, Ming-Liang ; Ma, Ding ; Guo, Lin-Wei ; Pei, Yu-Chen ; Chai, Wen-Jun ; Li, Da-Qiang ; Bai, Fan ; Bertucci, François ; Hu, Xin ; Jiang, Yi-Zhou ; Shao, Zhi-Ming</creatorcontrib><description>Triple-negative breast cancer (TNBC) remains an unmet medical challenge. We investigated metabolic dysregulation in TNBCs by using our multi-omics database (n = 465, the largest to date). TNBC samples were classified into three heterogeneous metabolic-pathway-based subtypes (MPSs) with distinct metabolic features: MPS1, the lipogenic subtype with upregulated lipid metabolism; MPS2, the glycolytic subtype with upregulated carbohydrate and nucleotide metabolism; and MPS3, the mixed subtype with partial pathway dysregulation. These subtypes were validated by metabolomic profiling of 72 samples. These three subtypes had distinct prognoses, molecular subtype distributions, and genomic alterations. Moreover, MPS1 TNBCs were more sensitive to metabolic inhibitors targeting fatty acid synthesis, whereas MPS2 TNBCs showed higher sensitivity to inhibitors targeting glycolysis. Importantly, inhibition of lactate dehydrogenase could enhance tumor response to anti-PD-1 immunotherapy in MPS2 TNBCs. Collectively, our analysis demonstrated the metabolic heterogeneity of TNBCs and enabled the development of personalized therapies targeting unique tumor metabolic profiles.
[Display omitted]
•The metabolic reprogramming and heterogeneity of TNBC is systematically characterized•TNBCs are classified into three subtypes on the basis of metabolic pathways•Three subtypes show distinct sensitivities to various metabolic inhibitors•Inhibition of LDH enhances tumor response to anti-PD-1 immunotherapy in MPS2 TNBCs
Gong et al. reveal the metabolic heterogeneity of triple-negative breast cancer and identify three metabolic-pathway-based subtypes with distinct molecular features and sensitivities to various metabolic inhibitors. They find that inhibition of lactate dehydrogenase could enhance the anti-PD-1 immunotherapy response in a certain subtype of triple-negative breast cancer.</description><identifier>ISSN: 1550-4131</identifier><identifier>ISSN: 1932-7420</identifier><identifier>EISSN: 1932-7420</identifier><identifier>DOI: 10.1016/j.cmet.2020.10.012</identifier><identifier>PMID: 33181091</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Cancer ; Female ; glycolysis ; heterogeneity ; Humans ; Immunotherapy ; Life Sciences ; Mammary Neoplasms, Experimental - metabolism ; Mammary Neoplasms, Experimental - therapy ; metabolic inhibitor ; metabolic pathway ; metabolism ; Mice ; Mice, Inbred BALB C ; Middle Aged ; subtype ; survival ; Triple Negative Breast Neoplasms - metabolism ; Triple Negative Breast Neoplasms - therapy ; triple-negative breast cancer ; Tumor Cells, Cultured</subject><ispartof>Cell metabolism, 2021-01, Vol.33 (1), p.51-64.e9</ispartof><rights>2020 Elsevier Inc.</rights><rights>Copyright © 2020 Elsevier Inc. All rights reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c483t-cdcf93ec5b460094f5bc8125ed0fca33286bb37c17b7431a87dd7558fbfc468f3</citedby><cites>FETCH-LOGICAL-c483t-cdcf93ec5b460094f5bc8125ed0fca33286bb37c17b7431a87dd7558fbfc468f3</cites><orcidid>0000-0002-0157-0959 ; 0000-0002-5113-2332</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.cmet.2020.10.012$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33181091$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://amu.hal.science/hal-03623115$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Gong, Yue</creatorcontrib><creatorcontrib>Ji, Peng</creatorcontrib><creatorcontrib>Yang, Yun-Song</creatorcontrib><creatorcontrib>Xie, Shao</creatorcontrib><creatorcontrib>Yu, Tian-Jian</creatorcontrib><creatorcontrib>Xiao, Yi</creatorcontrib><creatorcontrib>Jin, Ming-Liang</creatorcontrib><creatorcontrib>Ma, Ding</creatorcontrib><creatorcontrib>Guo, Lin-Wei</creatorcontrib><creatorcontrib>Pei, Yu-Chen</creatorcontrib><creatorcontrib>Chai, Wen-Jun</creatorcontrib><creatorcontrib>Li, Da-Qiang</creatorcontrib><creatorcontrib>Bai, Fan</creatorcontrib><creatorcontrib>Bertucci, François</creatorcontrib><creatorcontrib>Hu, Xin</creatorcontrib><creatorcontrib>Jiang, Yi-Zhou</creatorcontrib><creatorcontrib>Shao, Zhi-Ming</creatorcontrib><title>Metabolic-Pathway-Based Subtyping of Triple-Negative Breast Cancer Reveals Potential Therapeutic Targets</title><title>Cell metabolism</title><addtitle>Cell Metab</addtitle><description>Triple-negative breast cancer (TNBC) remains an unmet medical challenge. We investigated metabolic dysregulation in TNBCs by using our multi-omics database (n = 465, the largest to date). TNBC samples were classified into three heterogeneous metabolic-pathway-based subtypes (MPSs) with distinct metabolic features: MPS1, the lipogenic subtype with upregulated lipid metabolism; MPS2, the glycolytic subtype with upregulated carbohydrate and nucleotide metabolism; and MPS3, the mixed subtype with partial pathway dysregulation. These subtypes were validated by metabolomic profiling of 72 samples. These three subtypes had distinct prognoses, molecular subtype distributions, and genomic alterations. Moreover, MPS1 TNBCs were more sensitive to metabolic inhibitors targeting fatty acid synthesis, whereas MPS2 TNBCs showed higher sensitivity to inhibitors targeting glycolysis. Importantly, inhibition of lactate dehydrogenase could enhance tumor response to anti-PD-1 immunotherapy in MPS2 TNBCs. Collectively, our analysis demonstrated the metabolic heterogeneity of TNBCs and enabled the development of personalized therapies targeting unique tumor metabolic profiles.
[Display omitted]
•The metabolic reprogramming and heterogeneity of TNBC is systematically characterized•TNBCs are classified into three subtypes on the basis of metabolic pathways•Three subtypes show distinct sensitivities to various metabolic inhibitors•Inhibition of LDH enhances tumor response to anti-PD-1 immunotherapy in MPS2 TNBCs
Gong et al. reveal the metabolic heterogeneity of triple-negative breast cancer and identify three metabolic-pathway-based subtypes with distinct molecular features and sensitivities to various metabolic inhibitors. They find that inhibition of lactate dehydrogenase could enhance the anti-PD-1 immunotherapy response in a certain subtype of triple-negative breast cancer.</description><subject>Animals</subject><subject>Cancer</subject><subject>Female</subject><subject>glycolysis</subject><subject>heterogeneity</subject><subject>Humans</subject><subject>Immunotherapy</subject><subject>Life Sciences</subject><subject>Mammary Neoplasms, Experimental - metabolism</subject><subject>Mammary Neoplasms, Experimental - therapy</subject><subject>metabolic inhibitor</subject><subject>metabolic pathway</subject><subject>metabolism</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Middle Aged</subject><subject>subtype</subject><subject>survival</subject><subject>Triple Negative Breast Neoplasms - metabolism</subject><subject>Triple Negative Breast Neoplasms - therapy</subject><subject>triple-negative breast cancer</subject><subject>Tumor Cells, Cultured</subject><issn>1550-4131</issn><issn>1932-7420</issn><issn>1932-7420</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUtv2zAQhIkiRfPqH8gh4DE9yOVDTyCXxGiaAm4TtO6ZWFJLm4ZsqSTlwv--FJzk2NMuBt8OFjOEXHE244yXnzczs8U4E0xMwoxx8Y6c8UaKrMoFO0l7UbAs55KfkvMQNozJUjbyAzmVktecNfyMrL9jBN13zmTPENd_4ZDdQ8CW_hp1PAxut6K9pUvvhg6zH7iC6PZI7z1CiHQOO4Oe_sQ9Qhfocx9xFx10dLlGDwOO0Rm6BL_CGC7Je5sg_PgyL8jvhy_L-WO2ePr6bX63yExey5iZ1thGoil0XjLW5LbQpuaiwJZZA1KKutRaVoZXusolh7pq26ooaqutycvaygvy6ei7hk4N3m3BH1QPTj3eLdSkpRCE5LzY88TeHNnB939GDFFtXTDYdbDDfgxKpB-qsqlzmVBxRI3vQ_Bo37w5U1MbaqOmNtTUxqSlNtLR9Yv_qLfYvp28xp-A2yOAKZG9Q6-CcZhCbZ1HE1Xbu__5_wMU3pt5</recordid><startdate>20210105</startdate><enddate>20210105</enddate><creator>Gong, Yue</creator><creator>Ji, Peng</creator><creator>Yang, Yun-Song</creator><creator>Xie, Shao</creator><creator>Yu, Tian-Jian</creator><creator>Xiao, Yi</creator><creator>Jin, Ming-Liang</creator><creator>Ma, Ding</creator><creator>Guo, Lin-Wei</creator><creator>Pei, Yu-Chen</creator><creator>Chai, Wen-Jun</creator><creator>Li, Da-Qiang</creator><creator>Bai, Fan</creator><creator>Bertucci, François</creator><creator>Hu, Xin</creator><creator>Jiang, Yi-Zhou</creator><creator>Shao, Zhi-Ming</creator><general>Elsevier Inc</general><general>Elsevier</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>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-0157-0959</orcidid><orcidid>https://orcid.org/0000-0002-5113-2332</orcidid></search><sort><creationdate>20210105</creationdate><title>Metabolic-Pathway-Based Subtyping of Triple-Negative Breast Cancer Reveals Potential Therapeutic Targets</title><author>Gong, Yue ; Ji, Peng ; Yang, Yun-Song ; Xie, Shao ; Yu, Tian-Jian ; Xiao, Yi ; Jin, Ming-Liang ; Ma, Ding ; Guo, Lin-Wei ; Pei, Yu-Chen ; Chai, Wen-Jun ; Li, Da-Qiang ; Bai, Fan ; Bertucci, François ; Hu, Xin ; Jiang, Yi-Zhou ; Shao, Zhi-Ming</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c483t-cdcf93ec5b460094f5bc8125ed0fca33286bb37c17b7431a87dd7558fbfc468f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Cancer</topic><topic>Female</topic><topic>glycolysis</topic><topic>heterogeneity</topic><topic>Humans</topic><topic>Immunotherapy</topic><topic>Life Sciences</topic><topic>Mammary Neoplasms, Experimental - metabolism</topic><topic>Mammary Neoplasms, Experimental - therapy</topic><topic>metabolic inhibitor</topic><topic>metabolic pathway</topic><topic>metabolism</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Middle Aged</topic><topic>subtype</topic><topic>survival</topic><topic>Triple Negative Breast Neoplasms - metabolism</topic><topic>Triple Negative Breast Neoplasms - therapy</topic><topic>triple-negative breast cancer</topic><topic>Tumor Cells, Cultured</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gong, Yue</creatorcontrib><creatorcontrib>Ji, Peng</creatorcontrib><creatorcontrib>Yang, Yun-Song</creatorcontrib><creatorcontrib>Xie, Shao</creatorcontrib><creatorcontrib>Yu, Tian-Jian</creatorcontrib><creatorcontrib>Xiao, Yi</creatorcontrib><creatorcontrib>Jin, Ming-Liang</creatorcontrib><creatorcontrib>Ma, Ding</creatorcontrib><creatorcontrib>Guo, Lin-Wei</creatorcontrib><creatorcontrib>Pei, Yu-Chen</creatorcontrib><creatorcontrib>Chai, Wen-Jun</creatorcontrib><creatorcontrib>Li, Da-Qiang</creatorcontrib><creatorcontrib>Bai, Fan</creatorcontrib><creatorcontrib>Bertucci, François</creatorcontrib><creatorcontrib>Hu, Xin</creatorcontrib><creatorcontrib>Jiang, Yi-Zhou</creatorcontrib><creatorcontrib>Shao, Zhi-Ming</creatorcontrib><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>Hyper Article en Ligne (HAL)</collection><jtitle>Cell metabolism</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gong, Yue</au><au>Ji, Peng</au><au>Yang, Yun-Song</au><au>Xie, Shao</au><au>Yu, Tian-Jian</au><au>Xiao, Yi</au><au>Jin, Ming-Liang</au><au>Ma, Ding</au><au>Guo, Lin-Wei</au><au>Pei, Yu-Chen</au><au>Chai, Wen-Jun</au><au>Li, Da-Qiang</au><au>Bai, Fan</au><au>Bertucci, François</au><au>Hu, Xin</au><au>Jiang, Yi-Zhou</au><au>Shao, Zhi-Ming</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Metabolic-Pathway-Based Subtyping of Triple-Negative Breast Cancer Reveals Potential Therapeutic Targets</atitle><jtitle>Cell metabolism</jtitle><addtitle>Cell Metab</addtitle><date>2021-01-05</date><risdate>2021</risdate><volume>33</volume><issue>1</issue><spage>51</spage><epage>64.e9</epage><pages>51-64.e9</pages><issn>1550-4131</issn><issn>1932-7420</issn><eissn>1932-7420</eissn><abstract>Triple-negative breast cancer (TNBC) remains an unmet medical challenge. We investigated metabolic dysregulation in TNBCs by using our multi-omics database (n = 465, the largest to date). TNBC samples were classified into three heterogeneous metabolic-pathway-based subtypes (MPSs) with distinct metabolic features: MPS1, the lipogenic subtype with upregulated lipid metabolism; MPS2, the glycolytic subtype with upregulated carbohydrate and nucleotide metabolism; and MPS3, the mixed subtype with partial pathway dysregulation. These subtypes were validated by metabolomic profiling of 72 samples. These three subtypes had distinct prognoses, molecular subtype distributions, and genomic alterations. Moreover, MPS1 TNBCs were more sensitive to metabolic inhibitors targeting fatty acid synthesis, whereas MPS2 TNBCs showed higher sensitivity to inhibitors targeting glycolysis. Importantly, inhibition of lactate dehydrogenase could enhance tumor response to anti-PD-1 immunotherapy in MPS2 TNBCs. Collectively, our analysis demonstrated the metabolic heterogeneity of TNBCs and enabled the development of personalized therapies targeting unique tumor metabolic profiles.
[Display omitted]
•The metabolic reprogramming and heterogeneity of TNBC is systematically characterized•TNBCs are classified into three subtypes on the basis of metabolic pathways•Three subtypes show distinct sensitivities to various metabolic inhibitors•Inhibition of LDH enhances tumor response to anti-PD-1 immunotherapy in MPS2 TNBCs
Gong et al. reveal the metabolic heterogeneity of triple-negative breast cancer and identify three metabolic-pathway-based subtypes with distinct molecular features and sensitivities to various metabolic inhibitors. They find that inhibition of lactate dehydrogenase could enhance the anti-PD-1 immunotherapy response in a certain subtype of triple-negative breast cancer.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>33181091</pmid><doi>10.1016/j.cmet.2020.10.012</doi><orcidid>https://orcid.org/0000-0002-0157-0959</orcidid><orcidid>https://orcid.org/0000-0002-5113-2332</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Cancer Female glycolysis heterogeneity Humans Immunotherapy Life Sciences Mammary Neoplasms, Experimental - metabolism Mammary Neoplasms, Experimental - therapy metabolic inhibitor metabolic pathway metabolism Mice Mice, Inbred BALB C Middle Aged subtype survival Triple Negative Breast Neoplasms - metabolism Triple Negative Breast Neoplasms - therapy triple-negative breast cancer Tumor Cells, Cultured |
title | Metabolic-Pathway-Based Subtyping of Triple-Negative Breast Cancer Reveals Potential Therapeutic Targets |
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