Dietary dicarboxylic acids provide a nonstorable alternative fat source that protects mice against obesity
Dicarboxylic fatty acids are generated in the liver and kidney in a minor pathway called fatty acid ω-oxidation. The effects of consuming dicarboxylic fatty acids as an alternative source of dietary fat have not been explored. Here, we fed dodecanedioic acid, a 12-carbon dicarboxylic (DC12), to mice...
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| Veröffentlicht in: | The Journal of clinical investigation Jg. 134; H. 12 |
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| Sprache: | Englisch |
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American Society for Clinical Investigation
15.06.2024
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| ISSN: | 1558-8238, 0021-9738, 1558-8238 |
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| Abstract | Dicarboxylic fatty acids are generated in the liver and kidney in a minor pathway called fatty acid ω-oxidation. The effects of consuming dicarboxylic fatty acids as an alternative source of dietary fat have not been explored. Here, we fed dodecanedioic acid, a 12-carbon dicarboxylic (DC12), to mice at 20% of daily caloric intake for 9 weeks. DC12 increased metabolic rate, reduced body fat, reduced liver fat, and improved glucose tolerance. We observed DC12-specific breakdown products in liver, kidney, muscle, heart, and brain, indicating that oral DC12 escaped first-pass liver metabolism and was utilized by many tissues. In tissues expressing the "a" isoform of acyl-CoA oxidase-1 (ACOX1), a key peroxisomal fatty acid oxidation enzyme, DC12 was chain shortened to the TCA cycle intermediate succinyl-CoA. In tissues with low peroxisomal fatty acid oxidation capacity, DC12 was oxidized by mitochondria. In vitro, DC12 was catabolized even by adipose tissue and was not stored intracellularly. We conclude that DC12 and other dicarboxylic acids may be useful for combatting obesity and for treating metabolic disorders. |
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| AbstractList | Dicarboxylic fatty acids are generated in the liver and kidney in a minor pathway called fatty acid ω-oxidation. The effects of consuming dicarboxylic fatty acids as an alternative source of dietary fat have not been explored. Here, we fed dodecanedioic acid, a 12-carbon dicarboxylic (DC12), to mice at 20% of daily caloric intake for 9 weeks. DC12 increased metabolic rate, reduced body fat, reduced liver fat, and improved glucose tolerance. We observed DC12-specific breakdown products in liver, kidney, muscle, heart, and brain, indicating that oral DC12 escaped first-pass liver metabolism and was utilized by many tissues. In tissues expressing the “a” isoform of acyl-CoA oxidase-1 (ACOX1), a key peroxisomal fatty acid oxidation enzyme, DC12 was chain shortened to the TCA cycle intermediate succinyl-CoA. In tissues with low peroxisomal fatty acid oxidation capacity, DC12 was oxidized by mitochondria. In vitro, DC12 was catabolized even by adipose tissue and was not stored intracellularly. We conclude that DC12 and other dicarboxylic acids may be useful for combatting obesity and for treating metabolic disorders.
Dicarboxylic acids serve as an alternative energy source that dramatically remodels metabolism in mice. Dicarboxylic fatty acids are generated in the liver and kidney in a minor pathway called fatty acid m-oxidation. The effects of consuming dicarboxylic fatty acids as an alternative source of dietary fat have not been explored. Here, we fed dodecanedioic acid, a 12-carbon dicarboxylic ([DC.sub.12]), to mice at 20% of daily caloric intake for 9 weeks. [DC.sub.12] increased metabolic rate, reduced body fat, reduced liver fat, and improved glucose tolerance. We observed [DC.sub.12]-specific breakdown products in liver, kidney, muscle, heart, and brain, indicating that oral [DC.sub.12] escaped first-pass liver metabolism and was utilized by many tissues. In tissues expressing the "a" isoform of acyl-CoA oxidase-1 (ACOX1), a key peroxisomal fatty acid oxidation enzyme, [DC.sub.12] was chain shortened to the TCA cycle intermediate succinyl-CoA. In tissues with low peroxisomal fatty acid oxidation capacity, [DC.sub.12] was oxidized by mitochondria. In vitro, [DC.sub.12] was catabolized even by adipose tissue and was not stored intracellularly. We conclude that [DC.sub.12] and other dicarboxylic acids may be useful for combatting obesity and for treating metabolic disorders. Dicarboxylic fatty acids are generated in the liver and kidney in a minor pathway called fatty acid ω-oxidation. The effects of consuming dicarboxylic fatty acids as an alternative source of dietary fat have not been explored. Here, we fed dodecanedioic acid, a 12-carbon dicarboxylic (DC12), to mice at 20% of daily caloric intake for 9 weeks. DC12 increased metabolic rate, reduced body fat, reduced liver fat, and improved glucose tolerance. We observed DC12-specific breakdown products in liver, kidney, muscle, heart, and brain, indicating that oral DC12 escaped first-pass liver metabolism and was utilized by many tissues. In tissues expressing the "a" isoform of acyl-CoA oxidase-1 (ACOX1), a key peroxisomal fatty acid oxidation enzyme, DC12 was chain shortened to the TCA cycle intermediate succinyl-CoA. In tissues with low peroxisomal fatty acid oxidation capacity, DC12 was oxidized by mitochondria. In vitro, DC12 was catabolized even by adipose tissue and was not stored intracellularly. We conclude that DC12 and other dicarboxylic acids may be useful for combatting obesity and for treating metabolic disorders.Dicarboxylic fatty acids are generated in the liver and kidney in a minor pathway called fatty acid ω-oxidation. The effects of consuming dicarboxylic fatty acids as an alternative source of dietary fat have not been explored. Here, we fed dodecanedioic acid, a 12-carbon dicarboxylic (DC12), to mice at 20% of daily caloric intake for 9 weeks. DC12 increased metabolic rate, reduced body fat, reduced liver fat, and improved glucose tolerance. We observed DC12-specific breakdown products in liver, kidney, muscle, heart, and brain, indicating that oral DC12 escaped first-pass liver metabolism and was utilized by many tissues. In tissues expressing the "a" isoform of acyl-CoA oxidase-1 (ACOX1), a key peroxisomal fatty acid oxidation enzyme, DC12 was chain shortened to the TCA cycle intermediate succinyl-CoA. In tissues with low peroxisomal fatty acid oxidation capacity, DC12 was oxidized by mitochondria. In vitro, DC12 was catabolized even by adipose tissue and was not stored intracellularly. We conclude that DC12 and other dicarboxylic acids may be useful for combatting obesity and for treating metabolic disorders. Dicarboxylic fatty acids are generated in the liver and kidney in a minor pathway called fatty acid ω-oxidation. The effects of consuming dicarboxylic fatty acids as an alternative source of dietary fat have not been explored. Here, we fed dodecanedioic acid, a 12-carbon dicarboxylic (DC12), to mice at 20% of daily caloric intake for 9 weeks. DC12 increased metabolic rate, reduced body fat, reduced liver fat, and improved glucose tolerance. We observed DC12-specific breakdown products in liver, kidney, muscle, heart, and brain, indicating that oral DC12 escaped first-pass liver metabolism and was utilized by many tissues. In tissues expressing the “a” isoform of acyl-CoA oxidase-1 (ACOX1), a key peroxisomal fatty acid oxidation enzyme, DC12 was chain shortened to the TCA cycle intermediate succinyl-CoA. In tissues with low peroxisomal fatty acid oxidation capacity, DC12 was oxidized by mitochondria. In vitro, DC12 was catabolized even by adipose tissue and was not stored intracellularly. We conclude that DC12 and other dicarboxylic acids may be useful for combatting obesity and for treating metabolic disorders. |
| Audience | Academic |
| Author | Goetzman, Eric S. Bons, Joanna Shah, Samah Rose, Jacob Schilling, Birgit Zhang, Bob B. Richert, Adam C. Rao, Krithika S. Zhang, Yuxun Silva Barbosa, Anne Pfister, Katherine E. Sims-Lucas, Sunder Dobrowolski, Steven F. Shiva, Sruti S. Schmidt, Alexandra V. Mullett, Steven J. Solo, Keaton J. Gelhaus, Stacy L. Bharathi, Sivakama S. |
| AuthorAffiliation | 3 Department of Pharmacology and Chemical Biology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA 2 The Buck Institute for Research on Aging, Novato, California, USA 1 Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA 5 Vascular Medicine Institute and 4 Health Sciences Mass Spectrometry Core, University of Pittsburgh, Pittsburgh, Pennsylvania, USA 6 Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA |
| AuthorAffiliation_xml | – name: 1 Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA – name: 5 Vascular Medicine Institute and – name: 4 Health Sciences Mass Spectrometry Core, University of Pittsburgh, Pittsburgh, Pennsylvania, USA – name: 2 The Buck Institute for Research on Aging, Novato, California, USA – name: 6 Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA – name: 3 Department of Pharmacology and Chemical Biology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA |
| Author_xml | – sequence: 1 givenname: Eric S. orcidid: 0000-0001-9476-309X surname: Goetzman fullname: Goetzman, Eric S. – sequence: 2 givenname: Bob B. surname: Zhang fullname: Zhang, Bob B. – sequence: 3 givenname: Yuxun surname: Zhang fullname: Zhang, Yuxun – sequence: 4 givenname: Sivakama S. surname: Bharathi fullname: Bharathi, Sivakama S. – sequence: 5 givenname: Joanna surname: Bons fullname: Bons, Joanna – sequence: 6 givenname: Jacob surname: Rose fullname: Rose, Jacob – sequence: 7 givenname: Samah surname: Shah fullname: Shah, Samah – sequence: 8 givenname: Keaton J. orcidid: 0000-0002-4212-4832 surname: Solo fullname: Solo, Keaton J. – sequence: 9 givenname: Alexandra V. surname: Schmidt fullname: Schmidt, Alexandra V. – sequence: 10 givenname: Adam C. surname: Richert fullname: Richert, Adam C. – sequence: 11 givenname: Steven J. surname: Mullett fullname: Mullett, Steven J. – sequence: 12 givenname: Stacy L. orcidid: 0000-0001-9083-6933 surname: Gelhaus fullname: Gelhaus, Stacy L. – sequence: 13 givenname: Krithika S. surname: Rao fullname: Rao, Krithika S. – sequence: 14 givenname: Sruti S. surname: Shiva fullname: Shiva, Sruti S. – sequence: 15 givenname: Katherine E. surname: Pfister fullname: Pfister, Katherine E. – sequence: 16 givenname: Anne surname: Silva Barbosa fullname: Silva Barbosa, Anne – sequence: 17 givenname: Sunder orcidid: 0000-0003-1908-4809 surname: Sims-Lucas fullname: Sims-Lucas, Sunder – sequence: 18 givenname: Steven F. surname: Dobrowolski fullname: Dobrowolski, Steven F. – sequence: 19 givenname: Birgit surname: Schilling fullname: Schilling, Birgit |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38687608$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1172_JCI181978 crossref_primary_10_1113_JP287121 crossref_primary_10_21856_j_PEP_2025_2_05 crossref_primary_10_1096_fj_202402108R crossref_primary_10_3390_biom14121508 crossref_primary_10_1016_j_biopha_2024_117505 crossref_primary_10_1016_j_cellsig_2025_111744 crossref_primary_10_1007_s12672_025_02737_3 crossref_primary_10_3168_jds_2024_25235 crossref_primary_10_3390_biom14091160 crossref_primary_10_34067_KID_0000000746 |
| Cites_doi | 10.1152/ajpgi.1989.256.4.G680 10.1016/S0022-2275(20)42775-0 10.1177/014860719602000138 10.1203/00006450-198310000-00013 10.1074/mcp.R114.046664 10.1016/0005-2760(90)90005-I 10.1016/j.celrep.2013.07.024 10.1016/j.cmet.2013.11.013 10.1681/ASN.0000000000000266 10.1038/nmeth.1806 10.1172/jci.insight.93626 10.1002/jcp.28467 10.1194/jlr.R067629 10.1016/j.isci.2018.03.012 10.1371/journal.pone.0193824 10.2337/dc10-0663 10.1016/0014-5793(81)81064-2 10.1074/jbc.M508479200 10.1177/014860719902300280 10.1042/BCJ20230041 10.1016/j.biochi.2013.09.019 10.15252/embr.201745124 10.1002/humu.20535 10.1016/j.molcel.2020.05.007 10.1194/jlr.R005959 10.1098/rsos.230109 10.1016/0005-2760(91)90022-A 10.1016/S0021-9258(18)49936-X 10.12998/wjcc.v9.i2.308 10.3390/biom10081174 10.1194/jlr.M300512-JLR200 10.1016/B978-0-444-59565-2.00028-9 10.1016/j.cmet.2017.03.006 10.1073/pnas.1218034110 10.1146/annurev-med-042220-012821 10.1007/s13197-022-05499-w 10.1016/0003-2697(85)90412-9 10.1007/s00018-021-03869-9 10.1038/s41467-020-19743-4 10.1093/jb/mvw067 10.1016/j.bbalip.2013.12.001 10.1177/0148607195019006498 10.3164/jcbn.22-73 10.1016/S0021-9258(18)81625-8 10.1016/j.celrep.2013.08.032 10.1074/jbc.M116.763532 10.1111/jcmm.15325 10.3389/fcell.2020.00690 10.3389/fendo.2012.00022 10.1152/ajpendo.1999.276.3.E497 10.1016/S0021-9258(19)88666-0 10.1016/0006-2952(92)90298-W 10.1002/hep.27780 10.1002/jimd.12440 10.1152/ajpendo.00503.2003 10.1186/s12964-016-0126-1 10.1016/S0026-0495(96)90047-5 10.1152/ajpregu.00337.2016 10.1016/j.bbrc.2007.06.059 10.1152/ajpendo.00631.2005 10.1074/jbc.M115.651737 10.1172/JCI120606 10.1016/S0304-4165(89)80007-8 10.1016/j.jdiacomp.2020.107795 10.1007/BF01805531 |
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| Keywords | Fatty acid oxidation Obesity Mitochondria Metabolism |
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| Snippet | Dicarboxylic fatty acids are generated in the liver and kidney in a minor pathway called fatty acid ω-oxidation. The effects of consuming dicarboxylic fatty... Dicarboxylic fatty acids are generated in the liver and kidney in a minor pathway called fatty acid m-oxidation. The effects of consuming dicarboxylic fatty... |
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| SubjectTerms | Acyl-CoA Oxidase - genetics Acyl-CoA Oxidase - metabolism Adipose Tissue - metabolism Amino acids Animals Carboxylic acids Care and treatment Dextrose Dicarboxylic Acids - administration & dosage Dicarboxylic Acids - metabolism Dicarboxylic Acids - pharmacology Dietary fat Dietary Fats - administration & dosage Dietary Fats - metabolism Dietary Fats - pharmacology Fatty acids Fatty Acids - metabolism Glucose Health aspects Liver Liver - metabolism Male Metabolism Mice Mice, Inbred C57BL Obesity Obesity - metabolism Obesity - prevention & control Oxidases Oxidation-Reduction Peroxisomes - metabolism Physiological aspects Testing Type 2 diabetes |
| Title | Dietary dicarboxylic acids provide a nonstorable alternative fat source that protects mice against obesity |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/38687608 https://www.proquest.com/docview/3049718972 https://pubmed.ncbi.nlm.nih.gov/PMC11178532 https://doaj.org/article/155ac11721df44de9a8a3d4c6058390e |
| Volume | 134 |
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