Frequent silencing of popeye domain-containing genes, BVES and POPDC3, is associated with promoter hypermethylation in gastric cancer
The Popeye domain-containing (POPDC) genes BVES, POPDC2 and POPDC3 encode proteins that regulate cell–cell adhesion and cell migration during development. Herein, we report the frequent downregulation of BVES and POPDC3 by promoter hypermethylation in gastric cancer. POPDC expression in 11 gastric c...
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| Veröffentlicht in: | Carcinogenesis (New York) 2010-09, Vol.31 (9), p.1685-1693 |
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| creator | Kim, Mirang Jang, Hay-Ran Haam, Keeok Kang, Tae-Wook Kim, Jeong-Hwan Kim, Seon-Young Noh, Seung-Moo Song, Kyu-Sang Cho, June-Sik Jeong, Hyun-Yong Kim, Jin Cheon Yoo, Hyang-Sook Kim, Yong Sung |
| description | The Popeye domain-containing (POPDC) genes BVES, POPDC2 and POPDC3 encode proteins that regulate cell–cell adhesion and cell migration during development. Herein, we report the frequent downregulation of BVES and POPDC3 by promoter hypermethylation in gastric cancer. POPDC expression in 11 gastric cancer cell lines and 96 paired gastric tumor and normal adjacent tissues was analyzed with quantitative reverse transcription–polymerase chain reaction. The methylation status of BVES and POPDC3 was analyzed with methylated DNA immunoprecipitation sequencing, bisulfite sequencing and pyrosequencing. Expression of BVES and POPDC3 was downregulated in 73% of the gastric cancer cell lines and in 69% (BVES) and 87% (POPDC3) of the gastric cancer tissues. The BVES and POPDC3 promoter regions were hypermethylated in the gastric cancer cell lines in which they were silenced. Combined treatment with a DNA methylation inhibitor and a histone deacetylase inhibitor strongly induced BVES and POPDC3 expression. BVES and POPDC3 were hypermethylated in 69% (BVES) and 64% (POPDC3) of the gastric cancer tissues. We knocked down POPDC3 expression with short hairpin RNAs and examined the consequences on cell migration and invasion. Knockdown of POPDC3 in SNU-216 cells caused increased cell migration and invasion. Thus, epigenetic inactivation of BVES and POPDC3 occurs frequently in gastric tumors and may promote gastric cancer cell migration and invasion. |
| doi_str_mv | 10.1093/carcin/bgq144 |
| format | Article |
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Herein, we report the frequent downregulation of BVES and POPDC3 by promoter hypermethylation in gastric cancer. POPDC expression in 11 gastric cancer cell lines and 96 paired gastric tumor and normal adjacent tissues was analyzed with quantitative reverse transcription–polymerase chain reaction. The methylation status of BVES and POPDC3 was analyzed with methylated DNA immunoprecipitation sequencing, bisulfite sequencing and pyrosequencing. Expression of BVES and POPDC3 was downregulated in 73% of the gastric cancer cell lines and in 69% (BVES) and 87% (POPDC3) of the gastric cancer tissues. The BVES and POPDC3 promoter regions were hypermethylated in the gastric cancer cell lines in which they were silenced. Combined treatment with a DNA methylation inhibitor and a histone deacetylase inhibitor strongly induced BVES and POPDC3 expression. BVES and POPDC3 were hypermethylated in 69% (BVES) and 64% (POPDC3) of the gastric cancer tissues. We knocked down POPDC3 expression with short hairpin RNAs and examined the consequences on cell migration and invasion. Knockdown of POPDC3 in SNU-216 cells caused increased cell migration and invasion. Thus, epigenetic inactivation of BVES and POPDC3 occurs frequently in gastric tumors and may promote gastric cancer cell migration and invasion.</description><identifier>ISSN: 0143-3334</identifier><identifier>EISSN: 1460-2180</identifier><identifier>DOI: 10.1093/carcin/bgq144</identifier><identifier>PMID: 20627872</identifier><identifier>CODEN: CRNGDP</identifier><language>eng</language><publisher>Oxford: Oxford University Press</publisher><subject>Apoptosis ; Biological and medical sciences ; Bisulfite ; Carcinogenesis, carcinogens and anticarcinogens ; Cell Adhesion ; Cell Adhesion Molecules - genetics ; Cell Line, Tumor ; Cell Movement ; Cell Proliferation ; DNA Methylation ; Epigenesis, Genetic ; Gastroenterology. Liver. Pancreas. Abdomen ; Gene Expression Regulation, Neoplastic ; Gene Silencing ; Histone Deacetylase Inhibitors - pharmacology ; Humans ; Medical sciences ; Membrane Proteins - genetics ; Muscle Proteins - genetics ; Promoter Regions, Genetic - genetics ; Reverse Transcriptase Polymerase Chain Reaction ; RNA, Messenger - genetics ; Stomach Neoplasms - genetics ; Stomach. Duodenum. Small intestine. Colon. Rectum. Anus ; Tumors</subject><ispartof>Carcinogenesis (New York), 2010-09, Vol.31 (9), p.1685-1693</ispartof><rights>2015 INIST-CNRS</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c463t-17c6e26705d228ab2c27f2d2a46af01c8af26d70aa1195e223a38cac98f0d1063</citedby><cites>FETCH-LOGICAL-c463t-17c6e26705d228ab2c27f2d2a46af01c8af26d70aa1195e223a38cac98f0d1063</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=23195931$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20627872$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kim, Mirang</creatorcontrib><creatorcontrib>Jang, Hay-Ran</creatorcontrib><creatorcontrib>Haam, Keeok</creatorcontrib><creatorcontrib>Kang, Tae-Wook</creatorcontrib><creatorcontrib>Kim, Jeong-Hwan</creatorcontrib><creatorcontrib>Kim, Seon-Young</creatorcontrib><creatorcontrib>Noh, Seung-Moo</creatorcontrib><creatorcontrib>Song, Kyu-Sang</creatorcontrib><creatorcontrib>Cho, June-Sik</creatorcontrib><creatorcontrib>Jeong, Hyun-Yong</creatorcontrib><creatorcontrib>Kim, Jin Cheon</creatorcontrib><creatorcontrib>Yoo, Hyang-Sook</creatorcontrib><creatorcontrib>Kim, Yong Sung</creatorcontrib><title>Frequent silencing of popeye domain-containing genes, BVES and POPDC3, is associated with promoter hypermethylation in gastric cancer</title><title>Carcinogenesis (New York)</title><addtitle>Carcinogenesis</addtitle><description>The Popeye domain-containing (POPDC) genes BVES, POPDC2 and POPDC3 encode proteins that regulate cell–cell adhesion and cell migration during development. Herein, we report the frequent downregulation of BVES and POPDC3 by promoter hypermethylation in gastric cancer. POPDC expression in 11 gastric cancer cell lines and 96 paired gastric tumor and normal adjacent tissues was analyzed with quantitative reverse transcription–polymerase chain reaction. The methylation status of BVES and POPDC3 was analyzed with methylated DNA immunoprecipitation sequencing, bisulfite sequencing and pyrosequencing. Expression of BVES and POPDC3 was downregulated in 73% of the gastric cancer cell lines and in 69% (BVES) and 87% (POPDC3) of the gastric cancer tissues. The BVES and POPDC3 promoter regions were hypermethylated in the gastric cancer cell lines in which they were silenced. Combined treatment with a DNA methylation inhibitor and a histone deacetylase inhibitor strongly induced BVES and POPDC3 expression. BVES and POPDC3 were hypermethylated in 69% (BVES) and 64% (POPDC3) of the gastric cancer tissues. We knocked down POPDC3 expression with short hairpin RNAs and examined the consequences on cell migration and invasion. Knockdown of POPDC3 in SNU-216 cells caused increased cell migration and invasion. Thus, epigenetic inactivation of BVES and POPDC3 occurs frequently in gastric tumors and may promote gastric cancer cell migration and invasion.</description><subject>Apoptosis</subject><subject>Biological and medical sciences</subject><subject>Bisulfite</subject><subject>Carcinogenesis, carcinogens and anticarcinogens</subject><subject>Cell Adhesion</subject><subject>Cell Adhesion Molecules - genetics</subject><subject>Cell Line, Tumor</subject><subject>Cell Movement</subject><subject>Cell Proliferation</subject><subject>DNA Methylation</subject><subject>Epigenesis, Genetic</subject><subject>Gastroenterology. Liver. Pancreas. Abdomen</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Gene Silencing</subject><subject>Histone Deacetylase Inhibitors - pharmacology</subject><subject>Humans</subject><subject>Medical sciences</subject><subject>Membrane Proteins - genetics</subject><subject>Muscle Proteins - genetics</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>RNA, Messenger - genetics</subject><subject>Stomach Neoplasms - genetics</subject><subject>Stomach. Duodenum. Small intestine. Colon. Rectum. Anus</subject><subject>Tumors</subject><issn>0143-3334</issn><issn>1460-2180</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtvEzEUhS0EoqGwZIu8QWw61K-xZ5aQvqgqNeIlxMa68XgSw4w9tR3R_AD-N64S2iWs7uJ8OvfecxB6SclbSlp-bCAa54-XqxsqxCM0o0KSitGGPEYzQgWvOOfiAD1L6QchVPK6fYoOGJFMNYrN0O-zaG821mec3GB9sVrh0OMpTHZrcRdGcL4ywecy77SV9TYd4fdfTz9h8B1eXC9O5vwIu4QhpWAcZNvhXy6v8RTDGLKNeL2dbBxtXm8HyC547DxeQcrRGWzAGxufoyc9DMm-2M9D9OXs9PP8orq6Pv8wf3dVGSF5rqgy0jKpSN0x1sCSGaZ61jEQEnpCTQM9k50iAJS2tWWMA28MmLbpSUeJ5Ifozc633Fa-TlmPLhk7DOBt2CStZPElkvL_IpVqRPtvsuZt20gpClntSBNDStH2eopuhLjVlOi7MvWuTL0rs_Cv9s6b5Wi7e_pvewV4vQcgGRj6WMJ06YHjJYWW04fFLmV7e69D_Kml4qrWF9--64VoLz_WJ5e65n8A35u5Kg</recordid><startdate>20100901</startdate><enddate>20100901</enddate><creator>Kim, Mirang</creator><creator>Jang, Hay-Ran</creator><creator>Haam, Keeok</creator><creator>Kang, Tae-Wook</creator><creator>Kim, Jeong-Hwan</creator><creator>Kim, Seon-Young</creator><creator>Noh, Seung-Moo</creator><creator>Song, Kyu-Sang</creator><creator>Cho, June-Sik</creator><creator>Jeong, Hyun-Yong</creator><creator>Kim, Jin Cheon</creator><creator>Yoo, Hyang-Sook</creator><creator>Kim, Yong Sung</creator><general>Oxford University Press</general><scope>BSCLL</scope><scope>IQODW</scope><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><scope>7TM</scope><scope>7TO</scope><scope>H94</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope></search><sort><creationdate>20100901</creationdate><title>Frequent silencing of popeye domain-containing genes, BVES and POPDC3, is associated with promoter hypermethylation in gastric cancer</title><author>Kim, Mirang ; Jang, Hay-Ran ; Haam, Keeok ; Kang, Tae-Wook ; Kim, Jeong-Hwan ; Kim, Seon-Young ; Noh, Seung-Moo ; Song, Kyu-Sang ; Cho, June-Sik ; Jeong, Hyun-Yong ; Kim, Jin Cheon ; Yoo, Hyang-Sook ; Kim, Yong Sung</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c463t-17c6e26705d228ab2c27f2d2a46af01c8af26d70aa1195e223a38cac98f0d1063</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Apoptosis</topic><topic>Biological and medical sciences</topic><topic>Bisulfite</topic><topic>Carcinogenesis, carcinogens and anticarcinogens</topic><topic>Cell Adhesion</topic><topic>Cell Adhesion Molecules - genetics</topic><topic>Cell Line, Tumor</topic><topic>Cell Movement</topic><topic>Cell Proliferation</topic><topic>DNA Methylation</topic><topic>Epigenesis, Genetic</topic><topic>Gastroenterology. Liver. Pancreas. Abdomen</topic><topic>Gene Expression Regulation, Neoplastic</topic><topic>Gene Silencing</topic><topic>Histone Deacetylase Inhibitors - pharmacology</topic><topic>Humans</topic><topic>Medical sciences</topic><topic>Membrane Proteins - genetics</topic><topic>Muscle Proteins - genetics</topic><topic>Promoter Regions, Genetic - genetics</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>RNA, Messenger - genetics</topic><topic>Stomach Neoplasms - genetics</topic><topic>Stomach. Duodenum. Small intestine. Colon. Rectum. Anus</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kim, Mirang</creatorcontrib><creatorcontrib>Jang, Hay-Ran</creatorcontrib><creatorcontrib>Haam, Keeok</creatorcontrib><creatorcontrib>Kang, Tae-Wook</creatorcontrib><creatorcontrib>Kim, Jeong-Hwan</creatorcontrib><creatorcontrib>Kim, Seon-Young</creatorcontrib><creatorcontrib>Noh, Seung-Moo</creatorcontrib><creatorcontrib>Song, Kyu-Sang</creatorcontrib><creatorcontrib>Cho, June-Sik</creatorcontrib><creatorcontrib>Jeong, Hyun-Yong</creatorcontrib><creatorcontrib>Kim, Jin Cheon</creatorcontrib><creatorcontrib>Yoo, Hyang-Sook</creatorcontrib><creatorcontrib>Kim, Yong Sung</creatorcontrib><collection>Istex</collection><collection>Pascal-Francis</collection><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><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>Carcinogenesis (New York)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kim, Mirang</au><au>Jang, Hay-Ran</au><au>Haam, Keeok</au><au>Kang, Tae-Wook</au><au>Kim, Jeong-Hwan</au><au>Kim, Seon-Young</au><au>Noh, Seung-Moo</au><au>Song, Kyu-Sang</au><au>Cho, June-Sik</au><au>Jeong, Hyun-Yong</au><au>Kim, Jin Cheon</au><au>Yoo, Hyang-Sook</au><au>Kim, Yong Sung</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Frequent silencing of popeye domain-containing genes, BVES and POPDC3, is associated with promoter hypermethylation in gastric cancer</atitle><jtitle>Carcinogenesis (New York)</jtitle><addtitle>Carcinogenesis</addtitle><date>2010-09-01</date><risdate>2010</risdate><volume>31</volume><issue>9</issue><spage>1685</spage><epage>1693</epage><pages>1685-1693</pages><issn>0143-3334</issn><eissn>1460-2180</eissn><coden>CRNGDP</coden><abstract>The Popeye domain-containing (POPDC) genes BVES, POPDC2 and POPDC3 encode proteins that regulate cell–cell adhesion and cell migration during development. Herein, we report the frequent downregulation of BVES and POPDC3 by promoter hypermethylation in gastric cancer. POPDC expression in 11 gastric cancer cell lines and 96 paired gastric tumor and normal adjacent tissues was analyzed with quantitative reverse transcription–polymerase chain reaction. The methylation status of BVES and POPDC3 was analyzed with methylated DNA immunoprecipitation sequencing, bisulfite sequencing and pyrosequencing. Expression of BVES and POPDC3 was downregulated in 73% of the gastric cancer cell lines and in 69% (BVES) and 87% (POPDC3) of the gastric cancer tissues. The BVES and POPDC3 promoter regions were hypermethylated in the gastric cancer cell lines in which they were silenced. Combined treatment with a DNA methylation inhibitor and a histone deacetylase inhibitor strongly induced BVES and POPDC3 expression. BVES and POPDC3 were hypermethylated in 69% (BVES) and 64% (POPDC3) of the gastric cancer tissues. We knocked down POPDC3 expression with short hairpin RNAs and examined the consequences on cell migration and invasion. Knockdown of POPDC3 in SNU-216 cells caused increased cell migration and invasion. Thus, epigenetic inactivation of BVES and POPDC3 occurs frequently in gastric tumors and may promote gastric cancer cell migration and invasion.</abstract><cop>Oxford</cop><pub>Oxford University Press</pub><pmid>20627872</pmid><doi>10.1093/carcin/bgq144</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Carcinogenesis (New York), 2010-09, Vol.31 (9), p.1685-1693 |
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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Oxford University Press Journals All Titles (1996-Current); Alma/SFX Local Collection |
| subjects | Apoptosis Biological and medical sciences Bisulfite Carcinogenesis, carcinogens and anticarcinogens Cell Adhesion Cell Adhesion Molecules - genetics Cell Line, Tumor Cell Movement Cell Proliferation DNA Methylation Epigenesis, Genetic Gastroenterology. Liver. Pancreas. Abdomen Gene Expression Regulation, Neoplastic Gene Silencing Histone Deacetylase Inhibitors - pharmacology Humans Medical sciences Membrane Proteins - genetics Muscle Proteins - genetics Promoter Regions, Genetic - genetics Reverse Transcriptase Polymerase Chain Reaction RNA, Messenger - genetics Stomach Neoplasms - genetics Stomach. Duodenum. Small intestine. Colon. Rectum. Anus Tumors |
| title | Frequent silencing of popeye domain-containing genes, BVES and POPDC3, is associated with promoter hypermethylation in gastric cancer |
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