Comprehensive analysis of DNA methylation in head and neck squamous cell carcinoma indicates differences by survival and clinicopathologic characteristics
Head and neck squamous cell carcinoma (HNSCC) is the eighth most commonly diagnosed cancer in the United States. The risk of developing HNSCC increases with exposure to tobacco, alcohol and infection with human papilloma virus (HPV). HPV-associated HNSCCs have a distinct risk profile and improved pr...
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| creator | Colacino, Justin A Dolinoy, Dana C Duffy, Sonia A Sartor, Maureen A Chepeha, Douglas B Bradford, Carol R McHugh, Jonathan B Patel, Divya A Virani, Shama Walline, Heather M Bellile, Emily Terrell, Jeffrey E Stoerker, Jay A Taylor, Jeremy M G Carey, Thomas E Wolf, Gregory T Rozek, Laura S |
| description | Head and neck squamous cell carcinoma (HNSCC) is the eighth most commonly diagnosed cancer in the United States. The risk of developing HNSCC increases with exposure to tobacco, alcohol and infection with human papilloma virus (HPV). HPV-associated HNSCCs have a distinct risk profile and improved prognosis compared to cancers associated with tobacco and alcohol exposure. Epigenetic changes are an important mechanism in carcinogenic progression, but how these changes differ between viral- and chemical-induced cancers remains unknown. CpG methylation at 1505 CpG sites across 807 genes in 68 well-annotated HNSCC tumor samples from the University of Michigan Head and Neck SPORE patient population were quantified using the Illumina Goldengate Methylation Cancer Panel. Unsupervised hierarchical clustering based on methylation identified 6 distinct tumor clusters, which significantly differed by age, HPV status, and three year survival. Weighted linear modeling was used to identify differentially methylated genes based on epidemiological characteristics. Consistent with previous in vitro findings by our group, methylation of sites in the CCNA1 promoter was found to be higher in HPV(+) tumors, which was validated in an additional sample set of 128 tumors. After adjusting for cancer site, stage, age, gender, alcohol consumption, and smoking status, HPV status was found to be a significant predictor for DNA methylation at an additional 11 genes, including CASP8 and SYBL1. These findings provide insight into the epigenetic regulation of viral vs. chemical carcinogenesis and could provide novel targets for development of individualized therapeutic and prevention regimens based on environmental exposures. |
| doi_str_mv | 10.1371/journal.pone.0054742 |
| format | Article |
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The risk of developing HNSCC increases with exposure to tobacco, alcohol and infection with human papilloma virus (HPV). HPV-associated HNSCCs have a distinct risk profile and improved prognosis compared to cancers associated with tobacco and alcohol exposure. Epigenetic changes are an important mechanism in carcinogenic progression, but how these changes differ between viral- and chemical-induced cancers remains unknown. CpG methylation at 1505 CpG sites across 807 genes in 68 well-annotated HNSCC tumor samples from the University of Michigan Head and Neck SPORE patient population were quantified using the Illumina Goldengate Methylation Cancer Panel. Unsupervised hierarchical clustering based on methylation identified 6 distinct tumor clusters, which significantly differed by age, HPV status, and three year survival. Weighted linear modeling was used to identify differentially methylated genes based on epidemiological characteristics. Consistent with previous in vitro findings by our group, methylation of sites in the CCNA1 promoter was found to be higher in HPV(+) tumors, which was validated in an additional sample set of 128 tumors. After adjusting for cancer site, stage, age, gender, alcohol consumption, and smoking status, HPV status was found to be a significant predictor for DNA methylation at an additional 11 genes, including CASP8 and SYBL1. These findings provide insight into the epigenetic regulation of viral vs. chemical carcinogenesis and could provide novel targets for development of individualized therapeutic and prevention regimens based on environmental exposures.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0054742</identifier><identifier>PMID: 23358896</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Aged ; Aged, 80 and over ; Alcohol use ; Alcoholic beverages ; Base Sequence ; Biology ; Biomarkers ; Cancer ; Carcinogenesis ; Carcinogens ; Carcinoma, Squamous Cell - genetics ; Carcinoma, Squamous Cell - pathology ; Carcinoma, Squamous Cell - virology ; Care and treatment ; Cell cycle ; Cell survival ; Cluster Analysis ; Clustering ; CpG Islands ; Deoxyribonucleic acid ; Development and progression ; DNA ; DNA Methylation ; DNA Primers ; Environmental health ; Epidemiology ; Epigenetics ; Exposure ; Female ; Gene expression ; Genes ; Genetic aspects ; Genomics ; Genotypes ; Head ; Head & neck cancer ; Head and neck cancer ; Head and Neck Neoplasms - genetics ; Head and Neck Neoplasms - pathology ; Head and Neck Neoplasms - virology ; Health aspects ; Health risks ; Health sciences ; Human papillomavirus ; Humans ; Hybridization ; Male ; Medical research ; Medical schools ; Medicine ; Middle Aged ; Mutation ; Otolaryngology ; Patients ; Polymerase Chain Reaction ; Public health ; Risk assessment ; Smoking ; Squamous cell carcinoma ; Survival ; Survival Analysis ; Tobacco ; Tumors ; Viruses ; Young Adult</subject><ispartof>PloS one, 2013-01, Vol.8 (1), p.e54742</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Colacino 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.</rights><rights>2013 Colacino et al 2013 Colacino et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-ff073dc40a6daef5268cfb0388ae317b873d40a7f04d911fa788f6ea0a4f66603</citedby><cites>FETCH-LOGICAL-c758t-ff073dc40a6daef5268cfb0388ae317b873d40a7f04d911fa788f6ea0a4f66603</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/PMC3554647/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3554647/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23358896$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Ramqvist, Torbjörn</contributor><creatorcontrib>Colacino, Justin A</creatorcontrib><creatorcontrib>Dolinoy, Dana C</creatorcontrib><creatorcontrib>Duffy, Sonia A</creatorcontrib><creatorcontrib>Sartor, Maureen A</creatorcontrib><creatorcontrib>Chepeha, Douglas B</creatorcontrib><creatorcontrib>Bradford, Carol R</creatorcontrib><creatorcontrib>McHugh, Jonathan B</creatorcontrib><creatorcontrib>Patel, Divya A</creatorcontrib><creatorcontrib>Virani, Shama</creatorcontrib><creatorcontrib>Walline, Heather M</creatorcontrib><creatorcontrib>Bellile, Emily</creatorcontrib><creatorcontrib>Terrell, Jeffrey E</creatorcontrib><creatorcontrib>Stoerker, Jay A</creatorcontrib><creatorcontrib>Taylor, Jeremy M G</creatorcontrib><creatorcontrib>Carey, Thomas E</creatorcontrib><creatorcontrib>Wolf, Gregory T</creatorcontrib><creatorcontrib>Rozek, Laura S</creatorcontrib><title>Comprehensive analysis of DNA methylation in head and neck squamous cell carcinoma indicates differences by survival and clinicopathologic characteristics</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Head and neck squamous cell carcinoma (HNSCC) is the eighth most commonly diagnosed cancer in the United States. The risk of developing HNSCC increases with exposure to tobacco, alcohol and infection with human papilloma virus (HPV). HPV-associated HNSCCs have a distinct risk profile and improved prognosis compared to cancers associated with tobacco and alcohol exposure. Epigenetic changes are an important mechanism in carcinogenic progression, but how these changes differ between viral- and chemical-induced cancers remains unknown. CpG methylation at 1505 CpG sites across 807 genes in 68 well-annotated HNSCC tumor samples from the University of Michigan Head and Neck SPORE patient population were quantified using the Illumina Goldengate Methylation Cancer Panel. Unsupervised hierarchical clustering based on methylation identified 6 distinct tumor clusters, which significantly differed by age, HPV status, and three year survival. Weighted linear modeling was used to identify differentially methylated genes based on epidemiological characteristics. Consistent with previous in vitro findings by our group, methylation of sites in the CCNA1 promoter was found to be higher in HPV(+) tumors, which was validated in an additional sample set of 128 tumors. After adjusting for cancer site, stage, age, gender, alcohol consumption, and smoking status, HPV status was found to be a significant predictor for DNA methylation at an additional 11 genes, including CASP8 and SYBL1. These findings provide insight into the epigenetic regulation of viral vs. chemical carcinogenesis and could provide novel targets for development of individualized therapeutic and prevention regimens based on environmental exposures.</description><subject>Adult</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Alcohol use</subject><subject>Alcoholic beverages</subject><subject>Base Sequence</subject><subject>Biology</subject><subject>Biomarkers</subject><subject>Cancer</subject><subject>Carcinogenesis</subject><subject>Carcinogens</subject><subject>Carcinoma, Squamous Cell - genetics</subject><subject>Carcinoma, Squamous Cell - pathology</subject><subject>Carcinoma, Squamous Cell - virology</subject><subject>Care and treatment</subject><subject>Cell cycle</subject><subject>Cell survival</subject><subject>Cluster Analysis</subject><subject>Clustering</subject><subject>CpG Islands</subject><subject>Deoxyribonucleic acid</subject><subject>Development and progression</subject><subject>DNA</subject><subject>DNA Methylation</subject><subject>DNA Primers</subject><subject>Environmental health</subject><subject>Epidemiology</subject><subject>Epigenetics</subject><subject>Exposure</subject><subject>Female</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomics</subject><subject>Genotypes</subject><subject>Head</subject><subject>Head & neck cancer</subject><subject>Head and neck cancer</subject><subject>Head and Neck Neoplasms - genetics</subject><subject>Head and Neck Neoplasms - pathology</subject><subject>Head and Neck Neoplasms - virology</subject><subject>Health aspects</subject><subject>Health risks</subject><subject>Health sciences</subject><subject>Human papillomavirus</subject><subject>Humans</subject><subject>Hybridization</subject><subject>Male</subject><subject>Medical research</subject><subject>Medical schools</subject><subject>Medicine</subject><subject>Middle 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Edition</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</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>Colacino, Justin A</au><au>Dolinoy, Dana C</au><au>Duffy, Sonia A</au><au>Sartor, Maureen A</au><au>Chepeha, Douglas B</au><au>Bradford, Carol R</au><au>McHugh, Jonathan B</au><au>Patel, Divya A</au><au>Virani, Shama</au><au>Walline, Heather M</au><au>Bellile, Emily</au><au>Terrell, Jeffrey E</au><au>Stoerker, Jay A</au><au>Taylor, Jeremy M G</au><au>Carey, Thomas E</au><au>Wolf, Gregory T</au><au>Rozek, Laura S</au><au>Ramqvist, Torbjörn</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comprehensive analysis of DNA methylation in head and neck squamous cell carcinoma indicates differences by survival and clinicopathologic characteristics</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-01-24</date><risdate>2013</risdate><volume>8</volume><issue>1</issue><spage>e54742</spage><pages>e54742-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Head and neck squamous cell carcinoma (HNSCC) is the eighth most commonly diagnosed cancer in the United States. The risk of developing HNSCC increases with exposure to tobacco, alcohol and infection with human papilloma virus (HPV). HPV-associated HNSCCs have a distinct risk profile and improved prognosis compared to cancers associated with tobacco and alcohol exposure. Epigenetic changes are an important mechanism in carcinogenic progression, but how these changes differ between viral- and chemical-induced cancers remains unknown. CpG methylation at 1505 CpG sites across 807 genes in 68 well-annotated HNSCC tumor samples from the University of Michigan Head and Neck SPORE patient population were quantified using the Illumina Goldengate Methylation Cancer Panel. Unsupervised hierarchical clustering based on methylation identified 6 distinct tumor clusters, which significantly differed by age, HPV status, and three year survival. Weighted linear modeling was used to identify differentially methylated genes based on epidemiological characteristics. Consistent with previous in vitro findings by our group, methylation of sites in the CCNA1 promoter was found to be higher in HPV(+) tumors, which was validated in an additional sample set of 128 tumors. After adjusting for cancer site, stage, age, gender, alcohol consumption, and smoking status, HPV status was found to be a significant predictor for DNA methylation at an additional 11 genes, including CASP8 and SYBL1. These findings provide insight into the epigenetic regulation of viral vs. chemical carcinogenesis and could provide novel targets for development of individualized therapeutic and prevention regimens based on environmental exposures.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23358896</pmid><doi>10.1371/journal.pone.0054742</doi><tpages>e54742</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-01, Vol.8 (1), p.e54742 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1327869316 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adult Aged Aged, 80 and over Alcohol use Alcoholic beverages Base Sequence Biology Biomarkers Cancer Carcinogenesis Carcinogens Carcinoma, Squamous Cell - genetics Carcinoma, Squamous Cell - pathology Carcinoma, Squamous Cell - virology Care and treatment Cell cycle Cell survival Cluster Analysis Clustering CpG Islands Deoxyribonucleic acid Development and progression DNA DNA Methylation DNA Primers Environmental health Epidemiology Epigenetics Exposure Female Gene expression Genes Genetic aspects Genomics Genotypes Head Head & neck cancer Head and neck cancer Head and Neck Neoplasms - genetics Head and Neck Neoplasms - pathology Head and Neck Neoplasms - virology Health aspects Health risks Health sciences Human papillomavirus Humans Hybridization Male Medical research Medical schools Medicine Middle Aged Mutation Otolaryngology Patients Polymerase Chain Reaction Public health Risk assessment Smoking Squamous cell carcinoma Survival Survival Analysis Tobacco Tumors Viruses Young Adult |
| title | Comprehensive analysis of DNA methylation in head and neck squamous cell carcinoma indicates differences by survival and clinicopathologic characteristics |
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