Promoter Hypomethylation of EpCAM-Regulated Bone Morphogenetic Protein Gene Family in Recurrent Endometrial Cancer
Purpose: Epigenetic regulation by promoter methylation plays a key role in tumorigenesis. Our goal was to investigate whether altered DNA methylation signatures associated with oncogenic signaling delineate biomarkers predictive of endometrial cancer recurrence. Experimental Design: Methyl-CpG-captu...
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| Published in | Clinical cancer research Vol. 19; no. 22; pp. 6272 - 6285 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Philadelphia, PA
American Association for Cancer Research
15.11.2013
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| Subjects | |
| Online Access | Get full text |
| ISSN | 1078-0432 1557-3265 1557-3265 |
| DOI | 10.1158/1078-0432.CCR-13-1734 |
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| Abstract | Purpose: Epigenetic regulation by promoter methylation plays a key role in tumorigenesis. Our goal was to investigate whether altered DNA methylation signatures associated with oncogenic signaling delineate biomarkers predictive of endometrial cancer recurrence.
Experimental Design: Methyl-CpG-capture sequencing was used for global screening of aberrant DNA methylation in our endometrial cancer cohort, followed by validation in an independent The Cancer Genome Atlas (TCGA) cohort. Bioinformatics as well as functional analyses in vitro, using RNA interference (RNAi) knockdown, were performed to examine regulatory mechanisms of candidate gene expression and contribution to aggressive phenotype, such as epithelial–mesenchymal transition (EMT).
Results: We identified 2,302 hypermethylated loci in endometrial tumors compared with control samples. Bone morphogenetic protein (BMP) family genes, including BMP1, 2, 3, 4, and 7, were among the frequently hypermethylated loci. Interestingly, BMP2, 3, 4, and 7 were less methylated in primary tumors with subsequent recurrence and in patients with shorter disease-free interval compared with nonrecurrent tumors, which was validated and associated with poor survival in the TCGA cohort (BMP4, P = 0.009; BMP7, P = 0.007). Stimulation of endometrial cancer cells with epidermal growth factor (EGF) induced EMT and transcriptional activation of these genes, which was mediated by the epithelial cell adhesion molecule (EpCAM). EGF signaling was implicated in maintaining the promoters of candidate BMP genes in an active chromatin configuration and thus subject to transcriptional activation.
Conclusions: Hypomethylation signatures of candidate BMP genes associated with EpCAM-mediated expression present putative biomarkers predictive of poor survival in endometrial cancer. Clin Cancer Res; 19(22); 6272–85. ©2013 AACR. |
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| AbstractList | Epigenetic regulation by promoter methylation plays a key role in tumorigenesis. Our goal was to investigate whether altered DNA methylation signatures associated with oncogenic signaling delineate biomarkers predictive of endometrial cancer recurrence.PURPOSEEpigenetic regulation by promoter methylation plays a key role in tumorigenesis. Our goal was to investigate whether altered DNA methylation signatures associated with oncogenic signaling delineate biomarkers predictive of endometrial cancer recurrence.Methyl-CpG-capture sequencing was used for global screening of aberrant DNA methylation in our endometrial cancer cohort, followed by validation in an independent The Cancer Genome Atlas (TCGA) cohort. Bioinformatics as well as functional analyses in vitro, using RNA interference (RNAi) knockdown, were performed to examine regulatory mechanisms of candidate gene expression and contribution to aggressive phenotype, such as epithelial-mesenchymal transition (EMT).EXPERIMENTAL DESIGNMethyl-CpG-capture sequencing was used for global screening of aberrant DNA methylation in our endometrial cancer cohort, followed by validation in an independent The Cancer Genome Atlas (TCGA) cohort. Bioinformatics as well as functional analyses in vitro, using RNA interference (RNAi) knockdown, were performed to examine regulatory mechanisms of candidate gene expression and contribution to aggressive phenotype, such as epithelial-mesenchymal transition (EMT).We identified 2,302 hypermethylated loci in endometrial tumors compared with control samples. Bone morphogenetic protein (BMP) family genes, including BMP1, 2, 3, 4, and 7, were among the frequently hypermethylated loci. Interestingly, BMP2, 3, 4, and 7 were less methylated in primary tumors with subsequent recurrence and in patients with shorter disease-free interval compared with nonrecurrent tumors, which was validated and associated with poor survival in the TCGA cohort (BMP4, P = 0.009; BMP7, P = 0.007). Stimulation of endometrial cancer cells with epidermal growth factor (EGF) induced EMT and transcriptional activation of these genes, which was mediated by the epithelial cell adhesion molecule (EpCAM). EGF signaling was implicated in maintaining the promoters of candidate BMP genes in an active chromatin configuration and thus subject to transcriptional activation.RESULTSWe identified 2,302 hypermethylated loci in endometrial tumors compared with control samples. Bone morphogenetic protein (BMP) family genes, including BMP1, 2, 3, 4, and 7, were among the frequently hypermethylated loci. Interestingly, BMP2, 3, 4, and 7 were less methylated in primary tumors with subsequent recurrence and in patients with shorter disease-free interval compared with nonrecurrent tumors, which was validated and associated with poor survival in the TCGA cohort (BMP4, P = 0.009; BMP7, P = 0.007). Stimulation of endometrial cancer cells with epidermal growth factor (EGF) induced EMT and transcriptional activation of these genes, which was mediated by the epithelial cell adhesion molecule (EpCAM). EGF signaling was implicated in maintaining the promoters of candidate BMP genes in an active chromatin configuration and thus subject to transcriptional activation.Hypomethylation signatures of candidate BMP genes associated with EpCAM-mediated expression present putative biomarkers predictive of poor survival in endometrial cancer.CONCLUSIONSHypomethylation signatures of candidate BMP genes associated with EpCAM-mediated expression present putative biomarkers predictive of poor survival in endometrial cancer. Epigenetic regulation by promoter methylation plays a key role in tumorigenesis. Our goal was to investigate whether altered DNA methylation signatures associated with oncogenic signaling delineate biomarkers predictive of endometrial cancer recurrence. Methyl-CpG-capture sequencing was used for global screening of aberrant DNA methylation in our endometrial cancer cohort, followed by validation in an independent The Cancer Genome Atlas (TCGA) cohort. Bioinformatics as well as functional analyses in vitro, using RNA interference (RNAi) knockdown, were performed to examine regulatory mechanisms of candidate gene expression and contribution to aggressive phenotype, such as epithelial-mesenchymal transition (EMT). We identified 2,302 hypermethylated loci in endometrial tumors compared with control samples. Bone morphogenetic protein (BMP) family genes, including BMP1, 2, 3, 4, and 7, were among the frequently hypermethylated loci. Interestingly, BMP2, 3, 4, and 7 were less methylated in primary tumors with subsequent recurrence and in patients with shorter disease-free interval compared with nonrecurrent tumors, which was validated and associated with poor survival in the TCGA cohort (BMP4, P = 0.009; BMP7, P = 0.007). Stimulation of endometrial cancer cells with epidermal growth factor (EGF) induced EMT and transcriptional activation of these genes, which was mediated by the epithelial cell adhesion molecule (EpCAM). EGF signaling was implicated in maintaining the promoters of candidate BMP genes in an active chromatin configuration and thus subject to transcriptional activation. Hypomethylation signatures of candidate BMP genes associated with EpCAM-mediated expression present putative biomarkers predictive of poor survival in endometrial cancer. Purpose: Epigenetic regulation by promoter methylation plays a key role in tumorigenesis. Our goal was to investigate whether altered DNA methylation signatures associated with oncogenic signaling delineate biomarkers predictive of endometrial cancer recurrence.Experimental Design: Methyl-CpG-capture sequencing was used for global screening of aberrant DNA methylation in our endometrial cancer cohort, followed by validation in an independent The Cancer Genome Atlas (TCGA) cohort. Bioinformatics as well as functional analyses in vitro, using RNA interference (RNAi) knockdown, were performed to examine regulatory mechanisms of candidate gene expression and contribution to aggressive phenotype, such as epithelial-mesenchymal transition (EMT).Results: We identified 2,302 hypermethylated loci in endometrial tumors compared with control samples. Bone morphogenetic protein (BMP) family genes, including BMP1, 2, 3, 4, and 7, were among the frequently hypermethylated loci. Interestingly, BMP2, 3, 4, and 7 were less methylated in primary tumors with subsequent recurrence and in patients with shorter disease-free interval compared with nonrecurrent tumors, which was validated and associated with poor survival in the TCGA cohort (BMP4, P = 0.009; BMP7, P = 0.007). Stimulation of endometrial cancer cells with epidermal growth factor (EGF) induced EMT and transcriptional activation of these genes, which was mediated by the epithelial cell adhesion molecule (EpCAM). EGF signaling was implicated in maintaining the promoters of candidate BMP genes in an active chromatin configuration and thus subject to transcriptional activation.Conclusions: Hypomethylation signatures of candidate BMP genes associated with EpCAM-mediated expression present putative biomarkers predictive of poor survival in endometrial cancer. Clin Cancer Res; 19(22); 6272-85. [copy2013 AACR. Purpose: Epigenetic regulation by promoter methylation plays a key role in tumorigenesis. Our goal was to investigate whether altered DNA methylation signatures associated with oncogenic signaling delineate biomarkers predictive of endometrial cancer recurrence. Experimental Design: Methyl-CpG-capture sequencing was used for global screening of aberrant DNA methylation in our endometrial cancer cohort, followed by validation in an independent The Cancer Genome Atlas (TCGA) cohort. Bioinformatics as well as functional analyses in vitro, using RNA interference (RNAi) knockdown, were performed to examine regulatory mechanisms of candidate gene expression and contribution to aggressive phenotype, such as epithelial–mesenchymal transition (EMT). Results: We identified 2,302 hypermethylated loci in endometrial tumors compared with control samples. Bone morphogenetic protein (BMP) family genes, including BMP1, 2, 3, 4, and 7, were among the frequently hypermethylated loci. Interestingly, BMP2, 3, 4, and 7 were less methylated in primary tumors with subsequent recurrence and in patients with shorter disease-free interval compared with nonrecurrent tumors, which was validated and associated with poor survival in the TCGA cohort (BMP4, P = 0.009; BMP7, P = 0.007). Stimulation of endometrial cancer cells with epidermal growth factor (EGF) induced EMT and transcriptional activation of these genes, which was mediated by the epithelial cell adhesion molecule (EpCAM). EGF signaling was implicated in maintaining the promoters of candidate BMP genes in an active chromatin configuration and thus subject to transcriptional activation. Conclusions: Hypomethylation signatures of candidate BMP genes associated with EpCAM-mediated expression present putative biomarkers predictive of poor survival in endometrial cancer. Clin Cancer Res; 19(22); 6272–85. ©2013 AACR. |
| Author | Huang, Tim Hui-Ming Huang, Yi-Wen Liu, Joseph Ruan, Jianhua Wang, Chiou-Miin Hsu, Ya-Ting Thompson, Ian M. Jadhav, Rohit R. Chen, Chun-Liang Gu, Fei Mutch, David G. Lai, Hung-Cheng Kirma, Nameer B. Huang, Rui-Lan Goodfellow, Paul J. |
| AuthorAffiliation | 1 Department of Molecular Medicine/Institute of Biotechnology, University of Texas Health Science Center at San Antonio, TX 78229, USA 8 Department of Obstetrics and Gynecology, Ohio State University, Columbus, OH 43210, USA 3 Department of Computer Science, University of Texas at San Antonio, TX, 78249, USA 4 Institute of Biomedical Informatics, National Yang-Ming University, National Defense Medical Centre at Taipei, Taiwan, Republic of China 9 Department of Urology, University of Texas Health Science Center at San Antonio, TX 78229, USA 7 Department of Obstetrics and Gynecology, Washington University School of Medicine and Siteman Cancer Center, St. Louis, MO 63110, USA 10 Cancer Therapy and Research Center, University of Texas Health Science Center at San Antonio, USA 2 Department of Obstetrics and Gynecology, Medical College of Wisconsin, Milwaukee, WI 53226, USA 6 Laboratory of Epigenetics and Cancer Stem Cells, National Defense Medical Centre at Taipei, Taiwan, Republic of China 5 Depart |
| AuthorAffiliation_xml | – name: 10 Cancer Therapy and Research Center, University of Texas Health Science Center at San Antonio, USA – name: 7 Department of Obstetrics and Gynecology, Washington University School of Medicine and Siteman Cancer Center, St. Louis, MO 63110, USA – name: 8 Department of Obstetrics and Gynecology, Ohio State University, Columbus, OH 43210, USA – name: 4 Institute of Biomedical Informatics, National Yang-Ming University, National Defense Medical Centre at Taipei, Taiwan, Republic of China – name: 9 Department of Urology, University of Texas Health Science Center at San Antonio, TX 78229, USA – name: 5 Department of Obstetrics and Gynecology, Tri-Service General Hospital, National Defense Medical Centre at Taipei, Taiwan, Republic of China – name: 1 Department of Molecular Medicine/Institute of Biotechnology, University of Texas Health Science Center at San Antonio, TX 78229, USA – name: 2 Department of Obstetrics and Gynecology, Medical College of Wisconsin, Milwaukee, WI 53226, USA – name: 3 Department of Computer Science, University of Texas at San Antonio, TX, 78249, USA – name: 6 Laboratory of Epigenetics and Cancer Stem Cells, National Defense Medical Centre at Taipei, Taiwan, Republic of China |
| Author_xml | – sequence: 1 givenname: Ya-Ting surname: Hsu fullname: Hsu, Ya-Ting – sequence: 2 givenname: Fei surname: Gu fullname: Gu, Fei – sequence: 3 givenname: Yi-Wen surname: Huang fullname: Huang, Yi-Wen – sequence: 4 givenname: Joseph surname: Liu fullname: Liu, Joseph – sequence: 5 givenname: Jianhua surname: Ruan fullname: Ruan, Jianhua – sequence: 6 givenname: Rui-Lan surname: Huang fullname: Huang, Rui-Lan – sequence: 7 givenname: Chiou-Miin surname: Wang fullname: Wang, Chiou-Miin – sequence: 8 givenname: Chun-Liang surname: Chen fullname: Chen, Chun-Liang – sequence: 9 givenname: Rohit R. surname: Jadhav fullname: Jadhav, Rohit R. – sequence: 10 givenname: Hung-Cheng surname: Lai fullname: Lai, Hung-Cheng – sequence: 11 givenname: David G. surname: Mutch fullname: Mutch, David G. – sequence: 12 givenname: Paul J. surname: Goodfellow fullname: Goodfellow, Paul J. – sequence: 13 givenname: Ian M. surname: Thompson fullname: Thompson, Ian M. – sequence: 14 givenname: Nameer B. surname: Kirma fullname: Kirma, Nameer B. – sequence: 15 givenname: Tim Hui-Ming surname: Huang fullname: Huang, Tim Hui-Ming |
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| Keywords | Promoter Endometrium cancer Relapse Bone morphogenetic protein Uterine diseases Multigene family Malignant tumor Methylation Cancer Female genital diseases |
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| Snippet | Purpose: Epigenetic regulation by promoter methylation plays a key role in tumorigenesis. Our goal was to investigate whether altered DNA methylation... Epigenetic regulation by promoter methylation plays a key role in tumorigenesis. Our goal was to investigate whether altered DNA methylation signatures... |
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| SubjectTerms | Antigens, Neoplasm - genetics Antigens, Neoplasm - metabolism Antineoplastic agents Base Sequence Biological and medical sciences Bone Morphogenetic Proteins - genetics Cell Adhesion Molecules - genetics Cell Adhesion Molecules - metabolism Cell Line, Tumor CpG Islands - genetics Disease-Free Survival DNA Methylation Endometrial Neoplasms - genetics Epidermal Growth Factor - metabolism Epidermal Growth Factor - pharmacology Epithelial Cell Adhesion Molecule Epithelial-Mesenchymal Transition - drug effects Female Female genital diseases Gynecology. Andrology. Obstetrics Humans Medical sciences Multiple tumors. Solid tumors. Tumors in childhood (general aspects) Neoplasm Recurrence, Local - genetics Pharmacology. Drug treatments Promoter Regions, Genetic RNA Interference RNA, Small Interfering Sequence Analysis, DNA Survival Transcriptional Activation - drug effects Tumors |
| Title | Promoter Hypomethylation of EpCAM-Regulated Bone Morphogenetic Protein Gene Family in Recurrent Endometrial Cancer |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/24077349 https://www.proquest.com/docview/1459564063 https://www.proquest.com/docview/1551627390 https://pubmed.ncbi.nlm.nih.gov/PMC4080631 |
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