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High-Fat Diet Drives an Aggressive Pancreatic Cancer Phenotype
Emerging evidence indicates associations between high-fat diet (HFD), metabolic syndrome (MetS), and increased risk of pancreatic cancer. However, individual components of an HFD that increase cancer risk have not been isolated. In addition, a specific pattern of cytokine elevation by which MetS dri...
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| Published in: | The Journal of surgical research 2021-08, Vol.264, p.163-172 |
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| creator | Garcia, Denise I. Hurst, Katie E. Bradshaw, Alexandra Janakiraman, Harinarayanan Wang, Cindy Camp, E. Ramsay |
| description | Emerging evidence indicates associations between high-fat diet (HFD), metabolic syndrome (MetS), and increased risk of pancreatic cancer. However, individual components of an HFD that increase cancer risk have not been isolated. In addition, a specific pattern of cytokine elevation by which MetS drives pancreatic tumor progression is not well described. We hypothesized that oleic acid (OA), a major component of HFD, would augment pancreatic neoplastic processes.
An orthotopic pancreatic cancer model with Panc02 cells was used to compare the effect of low-fat diet to OA-based HFD on cancer progression. Tumors were quantitated, analyzed by immunohistochemistry. In addition, serum cytokine levels were quantitated. Proliferation, migration assays, and expression of epithelial-to-mesenchymal transition factors were evaluated on Panc02 and MiaPaCa-2 pancreatic cancer cells cultured in high concentrations of OA.
HFD tumor-bearing mice (n = 8) had an 18% weight increase (P |
| doi_str_mv | 10.1016/j.jss.2020.10.007 |
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An orthotopic pancreatic cancer model with Panc02 cells was used to compare the effect of low-fat diet to OA-based HFD on cancer progression. Tumors were quantitated, analyzed by immunohistochemistry. In addition, serum cytokine levels were quantitated. Proliferation, migration assays, and expression of epithelial-to-mesenchymal transition factors were evaluated on Panc02 and MiaPaCa-2 pancreatic cancer cells cultured in high concentrations of OA.
HFD tumor-bearing mice (n = 8) had an 18% weight increase (P < 0.001) and increased tumor burden (P < 0.05) compared with the low-fat diet tumor-bearing group (n = 6). HFD tumors had significantly increased angiogenesis (P < 0.001) and decreased apoptosis (P < 0.05). Serum of HFD mice demonstrated increased levels of glucagon and glucagon-like peptide-1. Two pancreatic cancer cell lines cultured in OA demonstrated significant increases in proliferation (P < 0.001) and a >2.5-fold increase in cell migration (P < 0.001) when treated with OA. Panc02 treated with OA had increased expression of epithelial-to-mesenchymal transition factors SNAI-1 (Snail) and Zeb-1(P < 0.01).
High-fat conditions in vitro and in vivo resulted in an aggressive pancreatic cancer phenotype. Our data support further investigations elucidating molecular pathways augmented by MetS conditions to identify novel therapeutic strategies for pancreatic cancer.
•A high-fat diet (HFD) with 60% oleic acid fatty acid results in diet-induced obesity in both tumor and nontumor-bearing mice.•Murine orthotopic pancreatic adenocarcinoma model treated with HFD results in more aggressive cancer phenotype.•In vitro treatment of pancreatic cancer cells with oleic acid results in increased proliferation, migration, and expression of epithelial to mesenchymal transition markers and decreased apoptosis.•In vitro culture of pancreatic cancer cells with oleic acid results in metabolic derangements consistent with those seen in metabolic syndrome.]]></description><identifier>ISSN: 0022-4804</identifier><identifier>EISSN: 1095-8673</identifier><identifier>DOI: 10.1016/j.jss.2020.10.007</identifier><identifier>PMID: 33838401</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adenocarcinoma - etiology ; Adenocarcinoma - pathology ; Animals ; Cell Line, Tumor - transplantation ; Culture Media - metabolism ; Diet, High-Fat - adverse effects ; Disease Models, Animal ; Epithelial-Mesenchymal Transition ; High-fat diet ; Humans ; Metabolic syndrome ; Metabolic Syndrome - complications ; Metabolic Syndrome - pathology ; Mice ; Obesity ; Oleic Acid - metabolism ; Pancreas - cytology ; Pancreas - pathology ; Pancreatic adenocarcinoma (PDAC) ; Pancreatic Neoplasms - etiology ; Pancreatic Neoplasms - pathology</subject><ispartof>The Journal of surgical research, 2021-08, Vol.264, p.163-172</ispartof><rights>2020</rights><rights>Published by Elsevier Inc.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c353t-37d15d96ad023c7cd07575f565e8d12ff958df0c2966402cdf590d42eb85cf2f3</citedby><cites>FETCH-LOGICAL-c353t-37d15d96ad023c7cd07575f565e8d12ff958df0c2966402cdf590d42eb85cf2f3</cites><orcidid>0000-0002-2519-3190 ; 0000-0002-6878-5727</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33838401$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Garcia, Denise I.</creatorcontrib><creatorcontrib>Hurst, Katie E.</creatorcontrib><creatorcontrib>Bradshaw, Alexandra</creatorcontrib><creatorcontrib>Janakiraman, Harinarayanan</creatorcontrib><creatorcontrib>Wang, Cindy</creatorcontrib><creatorcontrib>Camp, E. Ramsay</creatorcontrib><title>High-Fat Diet Drives an Aggressive Pancreatic Cancer Phenotype</title><title>The Journal of surgical research</title><addtitle>J Surg Res</addtitle><description><![CDATA[Emerging evidence indicates associations between high-fat diet (HFD), metabolic syndrome (MetS), and increased risk of pancreatic cancer. However, individual components of an HFD that increase cancer risk have not been isolated. In addition, a specific pattern of cytokine elevation by which MetS drives pancreatic tumor progression is not well described. We hypothesized that oleic acid (OA), a major component of HFD, would augment pancreatic neoplastic processes.
An orthotopic pancreatic cancer model with Panc02 cells was used to compare the effect of low-fat diet to OA-based HFD on cancer progression. Tumors were quantitated, analyzed by immunohistochemistry. In addition, serum cytokine levels were quantitated. Proliferation, migration assays, and expression of epithelial-to-mesenchymal transition factors were evaluated on Panc02 and MiaPaCa-2 pancreatic cancer cells cultured in high concentrations of OA.
HFD tumor-bearing mice (n = 8) had an 18% weight increase (P < 0.001) and increased tumor burden (P < 0.05) compared with the low-fat diet tumor-bearing group (n = 6). HFD tumors had significantly increased angiogenesis (P < 0.001) and decreased apoptosis (P < 0.05). Serum of HFD mice demonstrated increased levels of glucagon and glucagon-like peptide-1. Two pancreatic cancer cell lines cultured in OA demonstrated significant increases in proliferation (P < 0.001) and a >2.5-fold increase in cell migration (P < 0.001) when treated with OA. Panc02 treated with OA had increased expression of epithelial-to-mesenchymal transition factors SNAI-1 (Snail) and Zeb-1(P < 0.01).
High-fat conditions in vitro and in vivo resulted in an aggressive pancreatic cancer phenotype. Our data support further investigations elucidating molecular pathways augmented by MetS conditions to identify novel therapeutic strategies for pancreatic cancer.
•A high-fat diet (HFD) with 60% oleic acid fatty acid results in diet-induced obesity in both tumor and nontumor-bearing mice.•Murine orthotopic pancreatic adenocarcinoma model treated with HFD results in more aggressive cancer phenotype.•In vitro treatment of pancreatic cancer cells with oleic acid results in increased proliferation, migration, and expression of epithelial to mesenchymal transition markers and decreased apoptosis.•In vitro culture of pancreatic cancer cells with oleic acid results in metabolic derangements consistent with those seen in metabolic syndrome.]]></description><subject>Adenocarcinoma - etiology</subject><subject>Adenocarcinoma - pathology</subject><subject>Animals</subject><subject>Cell Line, Tumor - transplantation</subject><subject>Culture Media - metabolism</subject><subject>Diet, High-Fat - adverse effects</subject><subject>Disease Models, Animal</subject><subject>Epithelial-Mesenchymal Transition</subject><subject>High-fat diet</subject><subject>Humans</subject><subject>Metabolic syndrome</subject><subject>Metabolic Syndrome - complications</subject><subject>Metabolic Syndrome - pathology</subject><subject>Mice</subject><subject>Obesity</subject><subject>Oleic Acid - metabolism</subject><subject>Pancreas - cytology</subject><subject>Pancreas - pathology</subject><subject>Pancreatic adenocarcinoma (PDAC)</subject><subject>Pancreatic Neoplasms - etiology</subject><subject>Pancreatic Neoplasms - pathology</subject><issn>0022-4804</issn><issn>1095-8673</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kE9LAzEQxYMotlY_gBfZo5ddJ8lm_yAIpVoVCvag57BNJm2Wdrcm20K_vVlaPXqZmTe8eTA_Qm4pJBRo9lAntfcJA9brBCA_I0MKpYiLLOfnZAjAWJwWkA7Ilfc1BF3m_JIMOC94kQIdkqc3u1zF06qLni2G4uwefVQ10Xi5dOh9kNG8apTDqrMqmoQRXTRfYdN2hy1ekwtTrT3enPqIfE1fPidv8ezj9X0ynsWKC97FPNdU6DKrNDCucqUhF7kwIhNYaMqMKUWhDShWZlkKTGkjStApw0UhlGGGj8j9MXfr2u8d-k5urFe4XlcNtjsvmaCUpcBLEaz0aFWu9d6hkVtnN5U7SAqyxyZrGbDJHlu_CtjCzd0pfrfYoP67-OUUDI9HA4Yn9xad9MpiYKGtQ9VJ3dp_4n8A-cd79g</recordid><startdate>202108</startdate><enddate>202108</enddate><creator>Garcia, Denise I.</creator><creator>Hurst, Katie E.</creator><creator>Bradshaw, Alexandra</creator><creator>Janakiraman, Harinarayanan</creator><creator>Wang, Cindy</creator><creator>Camp, E. Ramsay</creator><general>Elsevier 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>7X8</scope><orcidid>https://orcid.org/0000-0002-2519-3190</orcidid><orcidid>https://orcid.org/0000-0002-6878-5727</orcidid></search><sort><creationdate>202108</creationdate><title>High-Fat Diet Drives an Aggressive Pancreatic Cancer Phenotype</title><author>Garcia, Denise I. ; Hurst, Katie E. ; Bradshaw, Alexandra ; Janakiraman, Harinarayanan ; Wang, Cindy ; Camp, E. Ramsay</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c353t-37d15d96ad023c7cd07575f565e8d12ff958df0c2966402cdf590d42eb85cf2f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adenocarcinoma - etiology</topic><topic>Adenocarcinoma - pathology</topic><topic>Animals</topic><topic>Cell Line, Tumor - transplantation</topic><topic>Culture Media - metabolism</topic><topic>Diet, High-Fat - adverse effects</topic><topic>Disease Models, Animal</topic><topic>Epithelial-Mesenchymal Transition</topic><topic>High-fat diet</topic><topic>Humans</topic><topic>Metabolic syndrome</topic><topic>Metabolic Syndrome - complications</topic><topic>Metabolic Syndrome - pathology</topic><topic>Mice</topic><topic>Obesity</topic><topic>Oleic Acid - metabolism</topic><topic>Pancreas - cytology</topic><topic>Pancreas - pathology</topic><topic>Pancreatic adenocarcinoma (PDAC)</topic><topic>Pancreatic Neoplasms - etiology</topic><topic>Pancreatic Neoplasms - pathology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Garcia, Denise I.</creatorcontrib><creatorcontrib>Hurst, Katie E.</creatorcontrib><creatorcontrib>Bradshaw, Alexandra</creatorcontrib><creatorcontrib>Janakiraman, Harinarayanan</creatorcontrib><creatorcontrib>Wang, Cindy</creatorcontrib><creatorcontrib>Camp, E. Ramsay</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><jtitle>The Journal of surgical research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Garcia, Denise I.</au><au>Hurst, Katie E.</au><au>Bradshaw, Alexandra</au><au>Janakiraman, Harinarayanan</au><au>Wang, Cindy</au><au>Camp, E. Ramsay</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>High-Fat Diet Drives an Aggressive Pancreatic Cancer Phenotype</atitle><jtitle>The Journal of surgical research</jtitle><addtitle>J Surg Res</addtitle><date>2021-08</date><risdate>2021</risdate><volume>264</volume><spage>163</spage><epage>172</epage><pages>163-172</pages><issn>0022-4804</issn><eissn>1095-8673</eissn><abstract><![CDATA[Emerging evidence indicates associations between high-fat diet (HFD), metabolic syndrome (MetS), and increased risk of pancreatic cancer. However, individual components of an HFD that increase cancer risk have not been isolated. In addition, a specific pattern of cytokine elevation by which MetS drives pancreatic tumor progression is not well described. We hypothesized that oleic acid (OA), a major component of HFD, would augment pancreatic neoplastic processes.
An orthotopic pancreatic cancer model with Panc02 cells was used to compare the effect of low-fat diet to OA-based HFD on cancer progression. Tumors were quantitated, analyzed by immunohistochemistry. In addition, serum cytokine levels were quantitated. Proliferation, migration assays, and expression of epithelial-to-mesenchymal transition factors were evaluated on Panc02 and MiaPaCa-2 pancreatic cancer cells cultured in high concentrations of OA.
HFD tumor-bearing mice (n = 8) had an 18% weight increase (P < 0.001) and increased tumor burden (P < 0.05) compared with the low-fat diet tumor-bearing group (n = 6). HFD tumors had significantly increased angiogenesis (P < 0.001) and decreased apoptosis (P < 0.05). Serum of HFD mice demonstrated increased levels of glucagon and glucagon-like peptide-1. Two pancreatic cancer cell lines cultured in OA demonstrated significant increases in proliferation (P < 0.001) and a >2.5-fold increase in cell migration (P < 0.001) when treated with OA. Panc02 treated with OA had increased expression of epithelial-to-mesenchymal transition factors SNAI-1 (Snail) and Zeb-1(P < 0.01).
High-fat conditions in vitro and in vivo resulted in an aggressive pancreatic cancer phenotype. Our data support further investigations elucidating molecular pathways augmented by MetS conditions to identify novel therapeutic strategies for pancreatic cancer.
•A high-fat diet (HFD) with 60% oleic acid fatty acid results in diet-induced obesity in both tumor and nontumor-bearing mice.•Murine orthotopic pancreatic adenocarcinoma model treated with HFD results in more aggressive cancer phenotype.•In vitro treatment of pancreatic cancer cells with oleic acid results in increased proliferation, migration, and expression of epithelial to mesenchymal transition markers and decreased apoptosis.•In vitro culture of pancreatic cancer cells with oleic acid results in metabolic derangements consistent with those seen in metabolic syndrome.]]></abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>33838401</pmid><doi>10.1016/j.jss.2020.10.007</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-2519-3190</orcidid><orcidid>https://orcid.org/0000-0002-6878-5727</orcidid></addata></record> |
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| subjects | Adenocarcinoma - etiology Adenocarcinoma - pathology Animals Cell Line, Tumor - transplantation Culture Media - metabolism Diet, High-Fat - adverse effects Disease Models, Animal Epithelial-Mesenchymal Transition High-fat diet Humans Metabolic syndrome Metabolic Syndrome - complications Metabolic Syndrome - pathology Mice Obesity Oleic Acid - metabolism Pancreas - cytology Pancreas - pathology Pancreatic adenocarcinoma (PDAC) Pancreatic Neoplasms - etiology Pancreatic Neoplasms - pathology |
| title | High-Fat Diet Drives an Aggressive Pancreatic Cancer Phenotype |
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