Functional interaction between acyl-CoA synthetase 4, lipooxygenases and cyclooxygenase-2 in the aggressive phenotype of breast cancer cells
The acyl-CoA synthetase 4 (ACSL4) is increased in breast cancer, colon and hepatocellular carcinoma. ACSL4 mainly esterifies arachidonic acid (AA) into arachidonoyl-CoA, reducing free AA intracellular levels, which is in contradiction with the need for AA metabolites in tumorigenesis. Therefore, the...
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Published in | PloS one Vol. 5; no. 11; p. e15540 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
11.11.2010
Public Library of Science (PLoS) |
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Abstract | The acyl-CoA synthetase 4 (ACSL4) is increased in breast cancer, colon and hepatocellular carcinoma. ACSL4 mainly esterifies arachidonic acid (AA) into arachidonoyl-CoA, reducing free AA intracellular levels, which is in contradiction with the need for AA metabolites in tumorigenesis. Therefore, the causal role of ACSL4 is still not established. This study was undertaken to determine the role of ACSL4 in AA metabolic pathway in breast cancer cells. The first novel finding is that ACSL4 regulates the expression of cyclooxygenase-2 (COX-2) and the production of prostaglandin in MDA-MB-231 cells. We also found that ACSL4 is significantly up-regulated in the highly aggressive MDA-MB-231 breast cancer cells. In terms of its overexpression and inhibition, ACSL4 plays a causal role in the control of the aggressive phenotype. These results were confirmed by the increase in the aggressive behaviour of MCF-7 cells stably transfected with a Tet-off ACSL4 vector. Concomitantly, another significant finding was that intramitochondrial AA levels are significantly higher in the aggressive cells. Thus, the esterification of AA by ACSL4 compartmentalizes the release of AA in mitochondria, a mechanism that serves to drive the specific lipooxygenase metabolization of the fatty acid. To our knowledge, this is the first report that ACSL4 expression controls both lipooxygenase and cyclooxygenase metabolism of AA. Thus, this functional interaction represents an integrated system that regulates the proliferating and metastatic potential of cancer cells. Therefore, the development of combinatory therapies that profit from the ACSL4, lipooxygenase and COX-2 synergistic action may allow for lower medication doses and avoidance of side effects. |
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AbstractList | The acyl-CoA synthetase 4 (ACSL4) is increased in breast cancer, colon and hepatocellular carcinoma. ACSL4 mainly esterifies arachidonic acid (AA) into arachidonoyl-CoA, reducing free AA intracellular levels, which is in contradiction with the need for AA metabolites in tumorigenesis. Therefore, the causal role of ACSL4 is still not established. This study was undertaken to determine the role of ACSL4 in AA metabolic pathway in breast cancer cells. The first novel finding is that ACSL4 regulates the expression of cyclooxygenase-2 (COX-2) and the production of prostaglandin in MDA-MB-231 cells. We also found that ACSL4 is significantly up-regulated in the highly aggressive MDA-MB-231 breast cancer cells. In terms of its overexpression and inhibition, ACSL4 plays a causal role in the control of the aggressive phenotype. These results were confirmed by the increase in the aggressive behaviour of MCF-7 cells stably transfected with a Tet-off ACSL4 vector. Concomitantly, another significant finding was that intramitochondrial AA levels are significantly higher in the aggressive cells. Thus, the esterification of AA by ACSL4 compartmentalizes the release of AA in mitochondria, a mechanism that serves to drive the specific lipooxygenase metabolization of the fatty acid. To our knowledge, this is the first report that ACSL4 expression controls both lipooxygenase and cyclooxygenase metabolism of AA. Thus, this functional interaction represents an integrated system that regulates the proliferating and metastatic potential of cancer cells. Therefore, the development of combinatory therapies that profit from the ACSL4, lipooxygenase and COX-2 synergistic action may allow for lower medication doses and avoidance of side effects. |
Audience | Academic |
Author | Orlando, Ulises D Maloberti, Paula M Pasqualini, María E Podestá, Ernesto J Solano, Angela R López-Otín, Carlos Duarte, Alejandra B |
AuthorAffiliation | University of Medicine and Dentistry of New Jersey, United States of America 2 Instituto de Biología Celular, School of Medicine, Córdoba National University, Córdoba, Argentina 1 Instituto de Investigaciones Moleculares de Enfermedades Hormonales Neurodegenerativas y Oncológicas (IIMHNO), Department of Human Biochemistry, School of Medicine, University of Buenos Aires, Buenos Aires, Argentina 3 Instituto Universitario de Oncología, Department of Biochemistry and Molecular Biology, Oviedo University, Oviedo, España |
AuthorAffiliation_xml | – name: University of Medicine and Dentistry of New Jersey, United States of America – name: 3 Instituto Universitario de Oncología, Department of Biochemistry and Molecular Biology, Oviedo University, Oviedo, España – name: 2 Instituto de Biología Celular, School of Medicine, Córdoba National University, Córdoba, Argentina – name: 1 Instituto de Investigaciones Moleculares de Enfermedades Hormonales Neurodegenerativas y Oncológicas (IIMHNO), Department of Human Biochemistry, School of Medicine, University of Buenos Aires, Buenos Aires, Argentina |
Author_xml | – sequence: 1 givenname: Paula M surname: Maloberti fullname: Maloberti, Paula M organization: Instituto de Investigaciones Moleculares de Enfermedades Hormonales Neurodegenerativas y Oncológicas, Department of Human Biochemistry, School of Medicine, University of Buenos Aires, Buenos Aires, Argentina – sequence: 2 givenname: Alejandra B surname: Duarte fullname: Duarte, Alejandra B – sequence: 3 givenname: Ulises D surname: Orlando fullname: Orlando, Ulises D – sequence: 4 givenname: María E surname: Pasqualini fullname: Pasqualini, María E – sequence: 5 givenname: Angela R surname: Solano fullname: Solano, Angela R – sequence: 6 givenname: Carlos surname: López-Otín fullname: López-Otín, Carlos – sequence: 7 givenname: Ernesto J surname: Podestá fullname: Podestá, Ernesto J |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21085606$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2010 Public Library of Science 2010 Maloberti et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Maloberti et al. 2010 |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: EJP CLO PMM. Performed the experiments: PMM ABD UDO MEP ÁRS. Analyzed the data: PMM ABD UDO MEP ÁRS CLO EJP. Contributed reagents/materials/analysis tools: EJP CLO PMM ÁRS. Wrote the paper: PMM CLO EJP. |
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Snippet | The acyl-CoA synthetase 4 (ACSL4) is increased in breast cancer, colon and hepatocellular carcinoma. ACSL4 mainly esterifies arachidonic acid (AA) into... |
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SubjectTerms | Aggressive behavior Antibiotics Apoptosis Arachidonate 12-Lipoxygenase - genetics Arachidonate 12-Lipoxygenase - metabolism Arachidonic acid Arachidonic Acid - metabolism Biochemistry Biology Biosynthesis Blotting, Western Breast cancer Breast Neoplasms - enzymology Breast Neoplasms - genetics Breast Neoplasms - pathology Cancer Cancer cells Cell cycle Cell growth Cell Line, Tumor Cell Movement Cell Proliferation Coenzyme A Ligases - genetics Coenzyme A Ligases - metabolism Colon Colon cancer COX-2 inhibitors Cyclooxygenase 2 - genetics Cyclooxygenase 2 - metabolism Cyclooxygenase-2 Drugs Enzymes Esterification Fatty acids Fatty Acids - metabolism Gene Expression Profiling Gene Expression Regulation, Enzymologic Gene Expression Regulation, Neoplastic Genetic aspects Genotype & phenotype Hepatocellular carcinoma Humans Intracellular levels Kinases Ligases Lipoxygenases - genetics Lipoxygenases - metabolism Liver cancer Medicine Metabolism Metabolites Metastases Metastasis Mitochondria Mitochondria - metabolism Motility Phosphorylation Physiological aspects Prostaglandins - metabolism Proteins Regulation Reverse Transcriptase Polymerase Chain Reaction RNA Interference Rodents Side effects Trends Tumorigenesis |
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Title | Functional interaction between acyl-CoA synthetase 4, lipooxygenases and cyclooxygenase-2 in the aggressive phenotype of breast cancer cells |
URI | https://www.ncbi.nlm.nih.gov/pubmed/21085606 https://www.proquest.com/docview/1295210098 https://search.proquest.com/docview/808462449 https://pubmed.ncbi.nlm.nih.gov/PMC2978721 https://doaj.org/article/905679b7612d4eb997f7f0540671069e http://dx.doi.org/10.1371/journal.pone.0015540 |
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