The Role of Dietary Extra Virgin Olive Oil and Corn Oil on the Alteration of Epigenetic Patterns in the Rat DMBA-Induced Breast Cancer Model
Disruption of epigenetic patterns is a major change occurring in all types of cancers. Such alterations are characterized by global DNA hypomethylation, gene-promoter hypermethylation and aberrant histone modifications, and may be modified by environment. Nutritional factors, and especially dietary...
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| description | Disruption of epigenetic patterns is a major change occurring in all types of cancers. Such alterations are characterized by global DNA hypomethylation, gene-promoter hypermethylation and aberrant histone modifications, and may be modified by environment. Nutritional factors, and especially dietary lipids, have a role in the etiology of breast cancer. Thus, we aimed to analyze the influence of different high fat diets on DNA methylation and histone modifications in the rat dimethylbenz(a)anthracene (DMBA)-induced breast cancer model. Female Sprague-Dawley rats were fed a low-fat, a high corn-oil or a high extra-virgin olive oil (EVOO) diet from weaning or from induction with DMBA. In mammary glands and tumors we analyzed global and gene specific (RASSF1A, TIMP3) DNA methylation by LUMA and bisulfite pyrosequencing assays, respectively. We also determined gene expression and enzymatic activity of DNA methyltransferases (DNMT1, DNMT3a and DNMT3b) and evaluated changes in histone modifications (H3K4me2, H3K27me3, H4K20me3 and H4K16ac) by western-blot. Our results showed variations along time in the global DNA methylation of the mammary gland displaying decreases at puberty and with aging. The olive oil-enriched diet, on the one hand, increased the levels of global DNA methylation in mammary gland and tumor, and on the other, changed histone modifications patterns. The corn oil-enriched diet increased DNA methyltransferase activity in both tissues, resulting in an increase in the promoter methylation of the tumor suppressor genes RASSF1A and TIMP3. These results suggest a differential effect of the high fat diets on epigenetic patterns with a relevant role in the neoplastic transformation, which could be one of the mechanisms of their differential promoter effect, clearly stimulating for the high corn-oil diet and with a weaker influence for the high EVOO diet, on breast cancer progression. |
| doi_str_mv | 10.1371/journal.pone.0138980 |
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Such alterations are characterized by global DNA hypomethylation, gene-promoter hypermethylation and aberrant histone modifications, and may be modified by environment. Nutritional factors, and especially dietary lipids, have a role in the etiology of breast cancer. Thus, we aimed to analyze the influence of different high fat diets on DNA methylation and histone modifications in the rat dimethylbenz(a)anthracene (DMBA)-induced breast cancer model. Female Sprague-Dawley rats were fed a low-fat, a high corn-oil or a high extra-virgin olive oil (EVOO) diet from weaning or from induction with DMBA. In mammary glands and tumors we analyzed global and gene specific (RASSF1A, TIMP3) DNA methylation by LUMA and bisulfite pyrosequencing assays, respectively. We also determined gene expression and enzymatic activity of DNA methyltransferases (DNMT1, DNMT3a and DNMT3b) and evaluated changes in histone modifications (H3K4me2, H3K27me3, H4K20me3 and H4K16ac) by western-blot. Our results showed variations along time in the global DNA methylation of the mammary gland displaying decreases at puberty and with aging. The olive oil-enriched diet, on the one hand, increased the levels of global DNA methylation in mammary gland and tumor, and on the other, changed histone modifications patterns. The corn oil-enriched diet increased DNA methyltransferase activity in both tissues, resulting in an increase in the promoter methylation of the tumor suppressor genes RASSF1A and TIMP3. These results suggest a differential effect of the high fat diets on epigenetic patterns with a relevant role in the neoplastic transformation, which could be one of the mechanisms of their differential promoter effect, clearly stimulating for the high corn-oil diet and with a weaker influence for the high EVOO diet, on breast cancer progression.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0138980</identifier><identifier>PMID: 26401660</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>9,10-Dimethyl-1,2-benzanthracene ; Aging ; Animals ; Anthracene ; Bisulfite ; Breast cancer ; Cancer ; Care and treatment ; Corn ; Corn oil ; Corn Oil - pharmacology ; Deoxyribonucleic acid ; Diet ; Diet, High-Fat ; Disease Models, Animal ; DNA ; DNA (Cytosine-5-)-Methyltransferases - genetics ; DNA (Cytosine-5-)-Methyltransferases - metabolism ; DNA methylation ; DNA Methylation - drug effects ; DNA methyltransferase ; DNMT1 protein ; Enzymatic activity ; Epigenesis, Genetic - drug effects ; Epigenetic inheritance ; Epigenetics ; Etiology ; Female ; Gene expression ; Gene Expression Regulation, Neoplastic - drug effects ; Genetic aspects ; Genetic transformation ; Health aspects ; High fat diet ; Histones - metabolism ; Lipids ; Mammary gland ; Mammary glands ; Mammary Neoplasms, Animal - chemically induced ; Mammary Neoplasms, Animal - genetics ; Mammary Neoplasms, Experimental - genetics ; Mammary Neoplasms, Experimental - pathology ; Oils & fats ; Olive oil ; Olive Oil - pharmacology ; Promoter Regions, Genetic - genetics ; Protein Processing, Post-Translational - drug effects ; Protein Processing, Post-Translational - genetics ; Puberty ; Rats, Sprague-Dawley ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Rodents ; Tissue inhibitor of metalloproteinase 3 ; Tissue Inhibitor of Metalloproteinase-3 - genetics ; Tissue Inhibitor of Metalloproteinase-3 - metabolism ; Transformation ; Tumor suppressor genes ; Tumor Suppressor Proteins - genetics ; Tumor Suppressor Proteins - metabolism ; Tumors ; Vegetables ; Weaning</subject><ispartof>PloS one, 2015-09, Vol.10 (9), p.e0138980-e0138980</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Rodríguez-Miguel et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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.</rights><rights>2015 Rodríguez-Miguel et al 2015 Rodríguez-Miguel et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-7a7e7b94e45033616c704b0bfb82b3fa9476c62c0913302888709c6d621679073</citedby><cites>FETCH-LOGICAL-c692t-7a7e7b94e45033616c704b0bfb82b3fa9476c62c0913302888709c6d621679073</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4581736/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4581736/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23865,27923,27924,53790,53792,79371,79372</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26401660$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Coleman, William B.</contributor><creatorcontrib>Rodríguez-Miguel, Cristina</creatorcontrib><creatorcontrib>Moral, Raquel</creatorcontrib><creatorcontrib>Escrich, Raquel</creatorcontrib><creatorcontrib>Vela, Elena</creatorcontrib><creatorcontrib>Solanas, Montserrat</creatorcontrib><creatorcontrib>Escrich, Eduard</creatorcontrib><title>The Role of Dietary Extra Virgin Olive Oil and Corn Oil on the Alteration of Epigenetic Patterns in the Rat DMBA-Induced Breast Cancer Model</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Disruption of epigenetic patterns is a major change occurring in all types of cancers. Such alterations are characterized by global DNA hypomethylation, gene-promoter hypermethylation and aberrant histone modifications, and may be modified by environment. Nutritional factors, and especially dietary lipids, have a role in the etiology of breast cancer. Thus, we aimed to analyze the influence of different high fat diets on DNA methylation and histone modifications in the rat dimethylbenz(a)anthracene (DMBA)-induced breast cancer model. Female Sprague-Dawley rats were fed a low-fat, a high corn-oil or a high extra-virgin olive oil (EVOO) diet from weaning or from induction with DMBA. In mammary glands and tumors we analyzed global and gene specific (RASSF1A, TIMP3) DNA methylation by LUMA and bisulfite pyrosequencing assays, respectively. We also determined gene expression and enzymatic activity of DNA methyltransferases (DNMT1, DNMT3a and DNMT3b) and evaluated changes in histone modifications (H3K4me2, H3K27me3, H4K20me3 and H4K16ac) by western-blot. Our results showed variations along time in the global DNA methylation of the mammary gland displaying decreases at puberty and with aging. The olive oil-enriched diet, on the one hand, increased the levels of global DNA methylation in mammary gland and tumor, and on the other, changed histone modifications patterns. The corn oil-enriched diet increased DNA methyltransferase activity in both tissues, resulting in an increase in the promoter methylation of the tumor suppressor genes RASSF1A and TIMP3. These results suggest a differential effect of the high fat diets on epigenetic patterns with a relevant role in the neoplastic transformation, which could be one of the mechanisms of their differential promoter effect, clearly stimulating for the high corn-oil diet and with a weaker influence for the high EVOO diet, on breast cancer progression.</description><subject>9,10-Dimethyl-1,2-benzanthracene</subject><subject>Aging</subject><subject>Animals</subject><subject>Anthracene</subject><subject>Bisulfite</subject><subject>Breast cancer</subject><subject>Cancer</subject><subject>Care and treatment</subject><subject>Corn</subject><subject>Corn oil</subject><subject>Corn Oil - pharmacology</subject><subject>Deoxyribonucleic acid</subject><subject>Diet</subject><subject>Diet, High-Fat</subject><subject>Disease Models, Animal</subject><subject>DNA</subject><subject>DNA (Cytosine-5-)-Methyltransferases - genetics</subject><subject>DNA (Cytosine-5-)-Methyltransferases - metabolism</subject><subject>DNA methylation</subject><subject>DNA Methylation - drug effects</subject><subject>DNA methyltransferase</subject><subject>DNMT1 protein</subject><subject>Enzymatic activity</subject><subject>Epigenesis, Genetic - drug effects</subject><subject>Epigenetic inheritance</subject><subject>Epigenetics</subject><subject>Etiology</subject><subject>Female</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Neoplastic - drug effects</subject><subject>Genetic aspects</subject><subject>Genetic transformation</subject><subject>Health aspects</subject><subject>High fat diet</subject><subject>Histones - metabolism</subject><subject>Lipids</subject><subject>Mammary gland</subject><subject>Mammary glands</subject><subject>Mammary Neoplasms, Animal - chemically induced</subject><subject>Mammary Neoplasms, Animal - genetics</subject><subject>Mammary Neoplasms, Experimental - genetics</subject><subject>Mammary Neoplasms, Experimental - pathology</subject><subject>Oils & fats</subject><subject>Olive oil</subject><subject>Olive Oil - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Rodríguez-Miguel, Cristina</au><au>Moral, Raquel</au><au>Escrich, Raquel</au><au>Vela, Elena</au><au>Solanas, Montserrat</au><au>Escrich, Eduard</au><au>Coleman, William B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Role of Dietary Extra Virgin Olive Oil and Corn Oil on the Alteration of Epigenetic Patterns in the Rat DMBA-Induced Breast Cancer Model</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-09-24</date><risdate>2015</risdate><volume>10</volume><issue>9</issue><spage>e0138980</spage><epage>e0138980</epage><pages>e0138980-e0138980</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Disruption of epigenetic patterns is a major change occurring in all types of cancers. Such alterations are characterized by global DNA hypomethylation, gene-promoter hypermethylation and aberrant histone modifications, and may be modified by environment. Nutritional factors, and especially dietary lipids, have a role in the etiology of breast cancer. Thus, we aimed to analyze the influence of different high fat diets on DNA methylation and histone modifications in the rat dimethylbenz(a)anthracene (DMBA)-induced breast cancer model. Female Sprague-Dawley rats were fed a low-fat, a high corn-oil or a high extra-virgin olive oil (EVOO) diet from weaning or from induction with DMBA. In mammary glands and tumors we analyzed global and gene specific (RASSF1A, TIMP3) DNA methylation by LUMA and bisulfite pyrosequencing assays, respectively. We also determined gene expression and enzymatic activity of DNA methyltransferases (DNMT1, DNMT3a and DNMT3b) and evaluated changes in histone modifications (H3K4me2, H3K27me3, H4K20me3 and H4K16ac) by western-blot. Our results showed variations along time in the global DNA methylation of the mammary gland displaying decreases at puberty and with aging. The olive oil-enriched diet, on the one hand, increased the levels of global DNA methylation in mammary gland and tumor, and on the other, changed histone modifications patterns. The corn oil-enriched diet increased DNA methyltransferase activity in both tissues, resulting in an increase in the promoter methylation of the tumor suppressor genes RASSF1A and TIMP3. These results suggest a differential effect of the high fat diets on epigenetic patterns with a relevant role in the neoplastic transformation, which could be one of the mechanisms of their differential promoter effect, clearly stimulating for the high corn-oil diet and with a weaker influence for the high EVOO diet, on breast cancer progression.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26401660</pmid><doi>10.1371/journal.pone.0138980</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2015-09, Vol.10 (9), p.e0138980-e0138980 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1719304902 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | 9,10-Dimethyl-1,2-benzanthracene Aging Animals Anthracene Bisulfite Breast cancer Cancer Care and treatment Corn Corn oil Corn Oil - pharmacology Deoxyribonucleic acid Diet Diet, High-Fat Disease Models, Animal DNA DNA (Cytosine-5-)-Methyltransferases - genetics DNA (Cytosine-5-)-Methyltransferases - metabolism DNA methylation DNA Methylation - drug effects DNA methyltransferase DNMT1 protein Enzymatic activity Epigenesis, Genetic - drug effects Epigenetic inheritance Epigenetics Etiology Female Gene expression Gene Expression Regulation, Neoplastic - drug effects Genetic aspects Genetic transformation Health aspects High fat diet Histones - metabolism Lipids Mammary gland Mammary glands Mammary Neoplasms, Animal - chemically induced Mammary Neoplasms, Animal - genetics Mammary Neoplasms, Experimental - genetics Mammary Neoplasms, Experimental - pathology Oils & fats Olive oil Olive Oil - pharmacology Promoter Regions, Genetic - genetics Protein Processing, Post-Translational - drug effects Protein Processing, Post-Translational - genetics Puberty Rats, Sprague-Dawley RNA, Messenger - genetics RNA, Messenger - metabolism Rodents Tissue inhibitor of metalloproteinase 3 Tissue Inhibitor of Metalloproteinase-3 - genetics Tissue Inhibitor of Metalloproteinase-3 - metabolism Transformation Tumor suppressor genes Tumor Suppressor Proteins - genetics Tumor Suppressor Proteins - metabolism Tumors Vegetables Weaning |
| title | The Role of Dietary Extra Virgin Olive Oil and Corn Oil on the Alteration of Epigenetic Patterns in the Rat DMBA-Induced Breast Cancer Model |
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