Identification of pre-diagnostic lipid sets associated with liver cancer risk using untargeted lipidomics and chemical set analysis: A nested case-control study within the ATBC cohort
In pre-disposed individuals, a reprogramming of the hepatic lipid metabolism may support liver cancer initiation. We conducted a high-resolution mass spectrometry based untargeted lipidomics analysis of pre-diagnostic serum samples from a nested case-control study (219 liver cancer cases and 219 con...
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| Veröffentlicht in: | International journal of cancer 2024-02, Vol.154 (3), p.454-464 |
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| container_title | International journal of cancer |
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| creator | Barupal, Dinesh K Ramos, Mark L Florio, Andrea A Wheeler, William A Weinstein, Stephanie J Albanes, Demetrius Fiehn, Oliver Graubard, Barry I Petrick, Jessica L McGlynn, Katherine A |
| description | In pre-disposed individuals, a reprogramming of the hepatic lipid metabolism may support liver cancer initiation. We conducted a high-resolution mass spectrometry based untargeted lipidomics analysis of pre-diagnostic serum samples from a nested case-control study (219 liver cancer cases and 219 controls) within the Alpha-Tocopherol, Beta-Carotene Cancer Prevention (ATBC) Study. Out of 462 annotated lipids, 158 (34.2%) were associated with liver cancer risk in a conditional logistic regression analysis at a false discovery rate (FDR) |
| doi_str_mv | 10.1002/ijc.34726 |
| format | Article |
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We conducted a high-resolution mass spectrometry based untargeted lipidomics analysis of pre-diagnostic serum samples from a nested case-control study (219 liver cancer cases and 219 controls) within the Alpha-Tocopherol, Beta-Carotene Cancer Prevention (ATBC) Study. Out of 462 annotated lipids, 158 (34.2%) were associated with liver cancer risk in a conditional logistic regression analysis at a false discovery rate (FDR) <0.05. A chemical set enrichment analysis (ChemRICH) and co-regulatory set analysis suggested that 22/28 lipid classes and 47/83 correlation modules were significantly associated with liver cancer risk (FDR <0.05). Strong positive associations were observed for monounsaturated fatty acids (MUFA), triacylglycerols (TAGs) and phosphatidylcholines (PCs) having MUFA acyl chains. Negative associations were observed for sphingolipids (ceramides and sphingomyelins), lysophosphatidylcholines, cholesterol esters and polyunsaturated fatty acids (PUFA) containing TAGs and PCs. Stearoyl-CoA desaturase enzyme 1 (SCD1), a rate limiting enzyme in fatty acid metabolism and ceramidases seems to be critical in this reprogramming. In conclusion, our study reports pre-diagnostic lipid changes that provide novel insights into hepatic lipid metabolism reprogramming may contribute to a pro-cell growth and anti-apoptotic tissue environment and, in turn, support liver cancer initiation.</description><identifier>ISSN: 0020-7136</identifier><identifier>EISSN: 1097-0215</identifier><identifier>DOI: 10.1002/ijc.34726</identifier><identifier>PMID: 37694774</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Apoptosis ; Cancer ; Case-Control Studies ; Cell growth ; Cholesterol ; Desaturase ; Enzymes ; Esters ; Fatty acids ; Fatty Acids, Monounsaturated ; Fatty Acids, Unsaturated ; Gas Chromatography-Mass Spectrometry ; Health risks ; Humans ; Lipid metabolism ; Lipidomics ; Lipids ; Liver cancer ; Liver Neoplasms - diagnosis ; Mass spectroscopy ; Medical research ; Metabolism ; Polyunsaturated fatty acids ; Regression analysis ; Sphingolipids ; Stearoyl-CoA Desaturase - metabolism ; Triglycerides</subject><ispartof>International journal of cancer, 2024-02, Vol.154 (3), p.454-464</ispartof><rights>2023 UICC.</rights><rights>2024 UICC</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c369t-8028c917e64f9273644b5fdd3c7889b36dde81dcda58ff5019ce252f71e6094e3</citedby><cites>FETCH-LOGICAL-c369t-8028c917e64f9273644b5fdd3c7889b36dde81dcda58ff5019ce252f71e6094e3</cites><orcidid>0000-0001-8330-4293 ; 0000-0002-9954-8628 ; 0000-0002-6261-8928 ; 0000-0001-6580-450X ; 0000-0003-2329-9933</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,781,785,886,27929,27930</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37694774$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Barupal, Dinesh K</creatorcontrib><creatorcontrib>Ramos, Mark L</creatorcontrib><creatorcontrib>Florio, Andrea A</creatorcontrib><creatorcontrib>Wheeler, William A</creatorcontrib><creatorcontrib>Weinstein, Stephanie J</creatorcontrib><creatorcontrib>Albanes, Demetrius</creatorcontrib><creatorcontrib>Fiehn, Oliver</creatorcontrib><creatorcontrib>Graubard, Barry I</creatorcontrib><creatorcontrib>Petrick, Jessica L</creatorcontrib><creatorcontrib>McGlynn, Katherine A</creatorcontrib><title>Identification of pre-diagnostic lipid sets associated with liver cancer risk using untargeted lipidomics and chemical set analysis: A nested case-control study within the ATBC cohort</title><title>International journal of cancer</title><addtitle>Int J Cancer</addtitle><description>In pre-disposed individuals, a reprogramming of the hepatic lipid metabolism may support liver cancer initiation. We conducted a high-resolution mass spectrometry based untargeted lipidomics analysis of pre-diagnostic serum samples from a nested case-control study (219 liver cancer cases and 219 controls) within the Alpha-Tocopherol, Beta-Carotene Cancer Prevention (ATBC) Study. Out of 462 annotated lipids, 158 (34.2%) were associated with liver cancer risk in a conditional logistic regression analysis at a false discovery rate (FDR) <0.05. A chemical set enrichment analysis (ChemRICH) and co-regulatory set analysis suggested that 22/28 lipid classes and 47/83 correlation modules were significantly associated with liver cancer risk (FDR <0.05). Strong positive associations were observed for monounsaturated fatty acids (MUFA), triacylglycerols (TAGs) and phosphatidylcholines (PCs) having MUFA acyl chains. Negative associations were observed for sphingolipids (ceramides and sphingomyelins), lysophosphatidylcholines, cholesterol esters and polyunsaturated fatty acids (PUFA) containing TAGs and PCs. Stearoyl-CoA desaturase enzyme 1 (SCD1), a rate limiting enzyme in fatty acid metabolism and ceramidases seems to be critical in this reprogramming. In conclusion, our study reports pre-diagnostic lipid changes that provide novel insights into hepatic lipid metabolism reprogramming may contribute to a pro-cell growth and anti-apoptotic tissue environment and, in turn, support liver cancer initiation.</description><subject>Apoptosis</subject><subject>Cancer</subject><subject>Case-Control Studies</subject><subject>Cell growth</subject><subject>Cholesterol</subject><subject>Desaturase</subject><subject>Enzymes</subject><subject>Esters</subject><subject>Fatty acids</subject><subject>Fatty Acids, Monounsaturated</subject><subject>Fatty Acids, Unsaturated</subject><subject>Gas Chromatography-Mass Spectrometry</subject><subject>Health risks</subject><subject>Humans</subject><subject>Lipid metabolism</subject><subject>Lipidomics</subject><subject>Lipids</subject><subject>Liver cancer</subject><subject>Liver Neoplasms - diagnosis</subject><subject>Mass spectroscopy</subject><subject>Medical research</subject><subject>Metabolism</subject><subject>Polyunsaturated fatty acids</subject><subject>Regression analysis</subject><subject>Sphingolipids</subject><subject>Stearoyl-CoA Desaturase - metabolism</subject><subject>Triglycerides</subject><issn>0020-7136</issn><issn>1097-0215</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdks-OFCEQxonRuOPqwRcwJF700Cs0dANeNuPEP5ts4mU9EwaqZxh7YAR6zTyZryc9u27UUxHqV18VxYfQS0ouKCHtO7-zF4yLtn-EFpQo0ZCWdo_RouZIIyjrz9CznHeEUNoR_hSdMdErLgRfoF9XDkLxg7em-BhwHPAhQeO82YSYi7d49AfvcIaSsck5Wm8KOPzTl21N3ULC1gRbQ_L5O56yDxs8hWLSBmbuVB333tbq4LDdQj2bcdarF2Y8Zp_f4yUOkGfcmgyNjaGkWJkyueOpkw-4bAEvbz6ssI3bmMpz9GQwY4YX9_Ecffv08Wb1pbn--vlqtbxuLOtVaSRppVVUQM8H1QrWc77uBueYFVKqNeudA0mddaaTw9ARqiy0XTsICj1RHNg5urzTPUzrPThbl5XMqA_J70066mi8_jcT_FZv4q2mRPKOsrYqvLlXSPHHVJ-p9z5bGEcTIE5Zt7Kv3yEJ7yv6-j90F6dUt1QpRYhkSnWz4Ns7yqaYc4LhYRpK9OwHXf2gT36o7Ku_x38g_xiA_QY8Z7Uj</recordid><startdate>20240201</startdate><enddate>20240201</enddate><creator>Barupal, Dinesh K</creator><creator>Ramos, Mark L</creator><creator>Florio, Andrea A</creator><creator>Wheeler, William A</creator><creator>Weinstein, Stephanie J</creator><creator>Albanes, Demetrius</creator><creator>Fiehn, Oliver</creator><creator>Graubard, Barry I</creator><creator>Petrick, Jessica L</creator><creator>McGlynn, Katherine A</creator><general>Wiley Subscription Services, Inc</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>7T5</scope><scope>7TO</scope><scope>7U9</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8330-4293</orcidid><orcidid>https://orcid.org/0000-0002-9954-8628</orcidid><orcidid>https://orcid.org/0000-0002-6261-8928</orcidid><orcidid>https://orcid.org/0000-0001-6580-450X</orcidid><orcidid>https://orcid.org/0000-0003-2329-9933</orcidid></search><sort><creationdate>20240201</creationdate><title>Identification of pre-diagnostic lipid sets associated with liver cancer risk using untargeted lipidomics and chemical set analysis: A nested case-control study within the ATBC cohort</title><author>Barupal, Dinesh K ; Ramos, Mark L ; Florio, Andrea A ; Wheeler, William A ; Weinstein, Stephanie J ; Albanes, Demetrius ; Fiehn, Oliver ; Graubard, Barry I ; Petrick, Jessica L ; McGlynn, Katherine A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c369t-8028c917e64f9273644b5fdd3c7889b36dde81dcda58ff5019ce252f71e6094e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Apoptosis</topic><topic>Cancer</topic><topic>Case-Control Studies</topic><topic>Cell growth</topic><topic>Cholesterol</topic><topic>Desaturase</topic><topic>Enzymes</topic><topic>Esters</topic><topic>Fatty acids</topic><topic>Fatty Acids, Monounsaturated</topic><topic>Fatty Acids, Unsaturated</topic><topic>Gas Chromatography-Mass Spectrometry</topic><topic>Health risks</topic><topic>Humans</topic><topic>Lipid metabolism</topic><topic>Lipidomics</topic><topic>Lipids</topic><topic>Liver cancer</topic><topic>Liver Neoplasms - diagnosis</topic><topic>Mass spectroscopy</topic><topic>Medical research</topic><topic>Metabolism</topic><topic>Polyunsaturated fatty acids</topic><topic>Regression analysis</topic><topic>Sphingolipids</topic><topic>Stearoyl-CoA Desaturase - metabolism</topic><topic>Triglycerides</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Barupal, Dinesh K</creatorcontrib><creatorcontrib>Ramos, Mark L</creatorcontrib><creatorcontrib>Florio, Andrea A</creatorcontrib><creatorcontrib>Wheeler, William A</creatorcontrib><creatorcontrib>Weinstein, Stephanie J</creatorcontrib><creatorcontrib>Albanes, Demetrius</creatorcontrib><creatorcontrib>Fiehn, Oliver</creatorcontrib><creatorcontrib>Graubard, Barry I</creatorcontrib><creatorcontrib>Petrick, Jessica L</creatorcontrib><creatorcontrib>McGlynn, Katherine A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>International journal of cancer</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Barupal, Dinesh K</au><au>Ramos, Mark L</au><au>Florio, Andrea A</au><au>Wheeler, William A</au><au>Weinstein, Stephanie J</au><au>Albanes, Demetrius</au><au>Fiehn, Oliver</au><au>Graubard, Barry I</au><au>Petrick, Jessica L</au><au>McGlynn, Katherine A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Identification of pre-diagnostic lipid sets associated with liver cancer risk using untargeted lipidomics and chemical set analysis: A nested case-control study within the ATBC cohort</atitle><jtitle>International journal of cancer</jtitle><addtitle>Int J Cancer</addtitle><date>2024-02-01</date><risdate>2024</risdate><volume>154</volume><issue>3</issue><spage>454</spage><epage>464</epage><pages>454-464</pages><issn>0020-7136</issn><eissn>1097-0215</eissn><abstract>In pre-disposed individuals, a reprogramming of the hepatic lipid metabolism may support liver cancer initiation. We conducted a high-resolution mass spectrometry based untargeted lipidomics analysis of pre-diagnostic serum samples from a nested case-control study (219 liver cancer cases and 219 controls) within the Alpha-Tocopherol, Beta-Carotene Cancer Prevention (ATBC) Study. Out of 462 annotated lipids, 158 (34.2%) were associated with liver cancer risk in a conditional logistic regression analysis at a false discovery rate (FDR) <0.05. A chemical set enrichment analysis (ChemRICH) and co-regulatory set analysis suggested that 22/28 lipid classes and 47/83 correlation modules were significantly associated with liver cancer risk (FDR <0.05). Strong positive associations were observed for monounsaturated fatty acids (MUFA), triacylglycerols (TAGs) and phosphatidylcholines (PCs) having MUFA acyl chains. Negative associations were observed for sphingolipids (ceramides and sphingomyelins), lysophosphatidylcholines, cholesterol esters and polyunsaturated fatty acids (PUFA) containing TAGs and PCs. Stearoyl-CoA desaturase enzyme 1 (SCD1), a rate limiting enzyme in fatty acid metabolism and ceramidases seems to be critical in this reprogramming. In conclusion, our study reports pre-diagnostic lipid changes that provide novel insights into hepatic lipid metabolism reprogramming may contribute to a pro-cell growth and anti-apoptotic tissue environment and, in turn, support liver cancer initiation.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>37694774</pmid><doi>10.1002/ijc.34726</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0001-8330-4293</orcidid><orcidid>https://orcid.org/0000-0002-9954-8628</orcidid><orcidid>https://orcid.org/0000-0002-6261-8928</orcidid><orcidid>https://orcid.org/0000-0001-6580-450X</orcidid><orcidid>https://orcid.org/0000-0003-2329-9933</orcidid></addata></record> |
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| subjects | Apoptosis Cancer Case-Control Studies Cell growth Cholesterol Desaturase Enzymes Esters Fatty acids Fatty Acids, Monounsaturated Fatty Acids, Unsaturated Gas Chromatography-Mass Spectrometry Health risks Humans Lipid metabolism Lipidomics Lipids Liver cancer Liver Neoplasms - diagnosis Mass spectroscopy Medical research Metabolism Polyunsaturated fatty acids Regression analysis Sphingolipids Stearoyl-CoA Desaturase - metabolism Triglycerides |
| title | Identification of pre-diagnostic lipid sets associated with liver cancer risk using untargeted lipidomics and chemical set analysis: A nested case-control study within the ATBC cohort |
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