Role for DNA Methylation in the Regulation of miR-200c and miR-141 Expression in Normal and Cancer Cells

Vrba, Lukas; Jensen, Taylor J.; Garbe, James C.; Heimark, Ronald L.; Cress, Anne E.; Dickinson, Sally; Stampfer, Martha R.; Futscher, Bernard W.

doi:10.1371/journal.pone.0008697

Title: Role for DNA Methylation in the Regulation of miR-200c and miR-141 Expression in Normal and Cancer Cells

Journal Article · 12 January 2010 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0008697 · OSTI ID:1627393

Vrba, Lukas ^[1]; Jensen, Taylor J. ^[2]; Garbe, James C. ^[3]; Heimark, Ronald L. ^[4]; Cress, Anne E. ^[4]; Dickinson, Sally ^[4]; Stampfer, Martha R. ^[5]; Futscher, Bernard W. ^[2]

Univ. of Arizona, Tucson, AZ (United States). Arizona Cancer Center; Inst. of Plant Molecular Biology, Ceske Budejovice (Czech Republic). Biology Centre ASCR; DOE/OSTI
Univ. of Arizona, Tucson, AZ (United States). Arizona Cancer Center; Univ. of Arizona, Tucson, AZ (United States). College of Pharmacy. Dept. of Pharmacology and Toxicology
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division
Univ. of Arizona, Tucson, AZ (United States). Arizona Cancer Center
Univ. of Arizona, Tucson, AZ (United States). Arizona Cancer Center; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division

Background: The microRNA-200 family participates in the maintenance of an epithelial phenotype and loss of its expression can result in epithelial to mesenchymal transition (EMT). Furthermore, the loss of expression of miR-200 family members is linked to an aggressive cancer phenotype. Regulation of the miR-200 family expression in normal and cancer cells is not fully understood. Methodology/Principal Findings: Epigenetic mechanisms participate in the control of miR-200c and miR-141 expression in both normal and cancer cells. A CpG island near the predicted mir-200c/mir-141 transcription start site shows a striking correlation between miR-200c and miR-141 expression and DNA methylation in both normal and cancer cells, as determined by Mass ARRAY technology. The CpG island is unmethylated in human miR-200/miR-141 expressing epithelial cells and in miR-200c/miR-141 positive tumor cells. The CpG island is heavily methylated in human miR-200c/miR-141 negative fibroblasts and miR-200c/miR-141 negative tumor cells. Mouse cells show a similar inverse correlation between DNA methylation and miR-200c expression. Enrichment of permissive histone modifications, H3 acetylation and H3K4 trimethylation, is seen in normal miR-200c/miR-141-positive epithelial cells, as determined by chromatin immunoprecipitation coupled to real-time PCR. In contrast, repressive H3K9 dimethylation marks are present in normal miR-200c/miR-141- negative fibroblasts and miR-200c/miR-141 negative cancer cells and the permissive histone modifications are absent. The epigenetic modifier drug, 5-aza-29-deoxycytidine, reactivates miR-200c/miR-141 expression showing that epigenetic mechanisms play a functional role in their transcriptional control. Conclusions/Significance: We report that DNA methylation plays a role in the normal cell type-specific expression of miR200c and miR-141 and this role appears evolutionarily conserved, since similar results were obtained in mouse. Aberrant DNA methylation of the miR-200c/141 CpG island is closely linked to their inappropriate silencing in cancer cells. Since the miR-200c cluster plays a significant role in EMT, our results suggest an important role for DNA methylation in the control of phenotypic conversions in normal cells.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC03-76SF00098

OSTI ID:: 1627393

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 1 Vol. 5; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (19)

Isolation of a human prostate carcinoma cell line (DU 145) Stone, Kenneth R.; Mickey, Don D.; Wunderli, Heidi International Journal of Cancer, Vol. 21, Issue 3 https://doi.org/10.1002/ijc.2910210305	journal	March 1978
The role of microRNAs in metastasis and epithelial-mesenchymal transition Bracken, C. P.; Gregory, P. A.; Khew-Goodall, Y. Cellular and Molecular Life Sciences, Vol. 66, Issue 10 https://doi.org/10.1007/s00018-009-8750-1	journal	January 2009
A species-generalized probabilistic model-based definition of CpG islands Irizarry, Rafael A.; Wu, Hao; Feinberg, Andrew P. Mammalian Genome, Vol. 20, Issue 9-10 https://doi.org/10.1007/s00335-009-9222-5	journal	September 2009
CpG Islands in vertebrate genomes Gardiner-Garden, M.; Frommer, M. Journal of Molecular Biology, Vol. 196, Issue 2 https://doi.org/10.1016/0022-2836(87)90689-9	journal	July 1987
Downregulation of miRNA-200c Links Breast Cancer Stem Cells with Normal Stem Cells Shimono, Yohei; Zabala, Maider; Cho, Robert W. Cell, Vol. 138, Issue 3 https://doi.org/10.1016/j.cell.2009.07.011	journal	August 2009
Large-scale human promoter mapping using CpG islands Ioshikhes, Ilya P.; Zhang, Michael Q. Nature Genetics, Vol. 26, Issue 1 https://doi.org/10.1038/79189	journal	September 2000
Role for DNA methylation in the control of cell type–specific maspin expression Futscher, Bernard W.; Oshiro, Marc M.; Wozniak, Ryan J. Nature Genetics, Vol. 31, Issue 2 https://doi.org/10.1038/ng886	journal	May 2002
Mutant p53 and aberrant cytosine methylation cooperate to silence gene expression Oshiro, Marc M.; Watts, George S.; Wozniak, Ryan J. Oncogene, Vol. 22, Issue 23 https://doi.org/10.1038/sj.onc.1206545	journal	June 2003
A microRNA expression signature of human solid tumors defines cancer gene targets Volinia, Stefano; Calin, George A.; Liu, Chang-Gong Proceedings of the National Academy of Sciences, Vol. 103, Issue 7 https://doi.org/10.1073/pnas.0510565103	journal	February 2006
Variants of 3T3 cells lacking mitogenic response to epidermal growth factor. Pruss, R. M.; Herschman, H. R. Proceedings of the National Academy of Sciences, Vol. 74, Issue 9 https://doi.org/10.1073/pnas.74.9.3918	journal	September 1977
Quantitative Studies of the Growth of Mouse Embryo Cells in Culture and Their Development into Established Lines Todaro, George J.; Green, Howard The Journal of Cell Biology, Vol. 17, Issue 2 https://doi.org/10.1083/jcb.17.2.299	journal	May 1963
Increased ROS levels contribute to elevated transcription factor and MAP kinase activities in malignantly progressed mouse keratinocyte cell lines Gupta, Ashok; Rosenberger, Sabine F.; Bowden, G. Tim Carcinogenesis, Vol. 20, Issue 11 https://doi.org/10.1093/carcin/20.11.2063	journal	November 1999
Murine Sarcoma and Leukemia Viruses: Assay Using Clonal Lines of Contact-Inhibited Mouse Cells Jainchill, John L.; Aaronson, Stuart A.; Todaro, George J. Journal of Virology, Vol. 4, Issue 5 https://doi.org/10.1128/jvi.4.5.549-553.1969	journal	November 1969
Overexpression of the MicroRNA hsa-miR-200c Leads to Reduced Expression of Transcription Factor 8 and Increased Expression of E-Cadherin Hurteau, Gregory J.; Carlson, J. Andrew; Spivack, Simon D. Cancer Research, Vol. 67, Issue 17 https://doi.org/10.1158/0008-5472.can-07-1058	journal	September 2007
MicroRNA Signatures in Human Ovarian Cancer Iorio, Marilena V.; Visone, Rosa; Di Leva, Gianpiero Cancer Research, Vol. 67, Issue 18 https://doi.org/10.1158/0008-5472.can-07-1936	journal	September 2007
CpGcluster: a distance-based algorithm for CpG-island detection Hackenberg, Michael; Previti, Christopher; Luque-Escamilla, Pedro Luis BMC Bioinformatics, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2105-7-446	journal	October 2006
Epigenetic Regulation of the Cell Type-Specific Gene 14-3-3σ M. ^Oshiro, Marc; Futscher, Bernard W.; Lisberg, Aaron Neoplasia, Vol. 7, Issue 9 https://doi.org/10.1593/neo.05274	journal	September 2005
miR-Q: a novel quantitative RT-PCR approach for the expression profiling of small RNA molecules such as miRNAs in a complex sample Sharbati-Tehrani, Soroush; Kutz-Lohroff, Barbara; Bergbauer, Ramona Freie Universität Berlin https://doi.org/10.17169/refubium-26590	text	January 2008
MiRNAs and Cancer Visone, Rosa; Croce, Carlo M. The American Journal of Pathology, Vol. 174, Issue 4 https://doi.org/10.2353/ajpath.2009.080794	journal	April 2009

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Concise Review: Stem Cells and Epithelial-Mesenchymal Transition in Cancer: Biological Implications and Therapeutic Targets: Stem Cells and EMT in Cancer Sato, Ryo; Semba, Takashi; Saya, Hideyuki STEM CELLS, Vol. 34, Issue 8 https://doi.org/10.1002/stem.2406	journal	June 2016
Epigenetics and MicroRNAs in Cancer Wise, Petra M.; Challagundla, Kishore B.; Fabbri, Muller Cancer Immunology, 479–489 https://doi.org/10.1007/978-3-030-30845-2_21	book	January 2020
Epigenetics and microRNAs in Cancer Wise, Petra M.; Challagundla, Kishore B.; Fabbri, Muller Cancer Immunology, 285–294 https://doi.org/10.1007/978-3-662-44006-3_16	book	August 2014
Relationship Between Noncoding RNA Dysregulation and Epigenetic Mechanisms in Cancer Suzuki, Hiromu; Maruyama, Reo; Yamamoto, Eiichiro Advances in Experimental Medicine and Biology, 109-135 https://doi.org/10.1007/978-981-10-1498-7_4	book	January 2016
lnflammation-induced epigenetic switches in cancer Rokavec, Matjaz; Öner, Meryem Gülfem; Hermeking, Heiko Cellular and Molecular Life Sciences, Vol. 73, Issue 1 https://doi.org/10.1007/s00018-015-2045-5	journal	September 2015
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miR-200c: a versatile watchdog in cancer progression, EMT, and drug resistance Mutlu, Merve; Raza, Umar; Saatci, Özge Journal of Molecular Medicine, Vol. 94, Issue 6 https://doi.org/10.1007/s00109-016-1420-5	journal	April 2016
miR-200bc/429 cluster modulates multidrug resistance of human cancer cell lines by targeting BCL2 and XIAP Zhu, Wei; Xu, Huaguo; Zhu, DanXia Cancer Chemotherapy and Pharmacology, Vol. 69, Issue 3 https://doi.org/10.1007/s00280-011-1752-3	journal	October 2011
Regulation of vascular endothelial growth factor signaling by miR-200b Choi, Young-Chul; Yoon, Sena; Jeong, Yongsu Molecules and Cells, Vol. 32, Issue 1 https://doi.org/10.1007/s10059-011-1042-2	journal	May 2011
The rejuvenated scenario of epithelial–mesenchymal transition (EMT) and cancer metastasis Meng, Fanyan; Wu, Guojun Cancer and Metastasis Reviews, Vol. 31, Issue 3-4 https://doi.org/10.1007/s10555-012-9379-3	journal	June 2012
The Pathophysiology of Epithelial-Mesenchymal Transition Induced by Transforming Growth Factor-β in Normal and Malignant Mammary Epithelial Cells Taylor, Molly A.; Parvani, Jenny G.; Schiemann, William P. Journal of Mammary Gland Biology and Neoplasia, Vol. 15, Issue 2 https://doi.org/10.1007/s10911-010-9181-1	journal	May 2010
The miR-200 and miR-221/222 microRNA Families: Opposing Effects on Epithelial Identity Howe, Erin N.; Cochrane, Dawn R.; Richer, Jennifer K. Journal of Mammary Gland Biology and Neoplasia, Vol. 17, Issue 1 https://doi.org/10.1007/s10911-012-9244-6	journal	February 2012
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DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer Lopez-Serra, P.; Esteller, M. Oncogene, Vol. 31, Issue 13 https://doi.org/10.1038/onc.2011.354	journal	August 2011
Dynamic epigenetic regulation of the microRNA-200 family mediates epithelial and mesenchymal transitions in human tumorigenesis Davalos, V.; Moutinho, C.; Villanueva, A. Oncogene, Vol. 31, Issue 16 https://doi.org/10.1038/onc.2011.383	journal	August 2011
Analysis of DNA methylation in single circulating tumor cells Pixberg, C. F.; Raba, K.; Müller, F. Oncogene, Vol. 36, Issue 23 https://doi.org/10.1038/onc.2016.480	journal	January 2017
ZEB1/NuRD complex suppresses TBC1D2b to stimulate E-cadherin internalization and promote metastasis in lung cancer Manshouri, Roxsan; Coyaud, Etienne; Kundu, Samrat T. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12832-z	journal	November 2019
Epigenetic silencing of microRNA-203 is required for EMT and cancer stem cell properties Taube, Joseph H.; Malouf, Gabriel G.; Lu, Emily Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep02687	journal	September 2013
miR-200a Regulates Nrf2 Activation by Targeting Keap1 mRNA in Breast Cancer Cells Eades, Gabriel; Yang, Muhua; Yao, Yuan Journal of Biological Chemistry, Vol. 286, Issue 47 https://doi.org/10.1074/jbc.m111.275495	journal	November 2011
DNA methylation biomarkers discovered in silico detect cancer in liquid biopsies from non-small cell lung cancer patients Vrba, Lukas; Oshiro, Marc M.; Kim, Samuel S. Epigenetics, Vol. 15, Issue 4 https://doi.org/10.1080/15592294.2019.1695333	journal	November 2019
An autocrine TGF-β/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition Gregory, Philip A.; Bracken, Cameron P.; Smith, Eric Molecular Biology of the Cell, Vol. 22, Issue 10 https://doi.org/10.1091/mbc.e11-02-0103	journal	May 2011
Methylation of microRNA genes regulates gene expression in bisexual flower development in andromonoecious poplar Song, Yuepeng; Tian, Min; Ci, Dong Journal of Experimental Botany, Vol. 66, Issue 7 https://doi.org/10.1093/jxb/eru531	journal	January 2015
Stable methylation of a non-coding RNA gene regulates gene expression in response to abiotic stress in Populus simonii Song, Yuepeng; Ci, Dong; Tian, Min Journal of Experimental Botany, Vol. 67, Issue 5 https://doi.org/10.1093/jxb/erv543	journal	December 2015
An integrative genomic approach identifies p73 and p63 as activators of miR-200 microRNA family transcription Knouf, Emily C.; Garg, Kavita; Arroyo, Jason D. Nucleic Acids Research, Vol. 40, Issue 2 https://doi.org/10.1093/nar/gkr731	journal	September 2011
Reversal and Prevention of Arsenic-Induced Human Bronchial Epithelial Cell Malignant Transformation by microRNA-200b Wang, Zhishan; Zhao, Yong; Smith, Eric Toxicological Sciences, Vol. 121, Issue 1 https://doi.org/10.1093/toxsci/kfr029	journal	February 2011
Integrated epigenome, exome and transcriptome analyses reveal molecular subtypes and homeotic transformation in uterine fibroids George, Jitu W.; Fan, Huihui; Johnson, Benjamin K. bioRxiv https://doi.org/10.1101/452342	posted_content	January 2018
MicroRNA 152 regulates hepatic glycogenesis by targeting PTEN Wang, Shuyue; Wang, Lilin; Dou, Lin The FEBS Journal, Vol. 283, Issue 10 https://doi.org/10.1111/febs.13713	journal	April 2016
miR-21a negatively modulates tumor suppressor genes PTEN and miR-200c and further promotes the transformation of M2 macrophages Li, Ning; Qin, Jun-Fang; Han, Xiao Immunology and Cell Biology, Vol. 96, Issue 1 https://doi.org/10.1111/imcb.1016	journal	December 2017
MicroRNAs and epigenetics: MicroRNAs and epigenetics Sato, Fumiaki; Tsuchiya, Soken; Meltzer, Stephen J. FEBS Journal, Vol. 278, Issue 10 https://doi.org/10.1111/j.1742-4658.2011.08089.x	journal	March 2011
MicroRNA-199a targets CD44 to suppress the tumorigenicity and multidrug resistance of ovarian cancer-initiating cells: MicroRNA-199a inhibits ovarian CIC growth Cheng, Weiwei; Liu, Te; Wan, Xiaoping FEBS Journal, Vol. 279, Issue 11 https://doi.org/10.1111/j.1742-4658.2012.08589.x	journal	April 2012
Suppression of MicroRNA 200 Family Expression by Oncogenic KRAS Activation Promotes Cell Survival and Epithelial-Mesenchymal Transition in KRAS-Driven Cancer Zhong, Xiaomin; Zheng, Lan; Shen, Jianfeng Molecular and Cellular Biology, Vol. 36, Issue 21 https://doi.org/10.1128/mcb.00079-16	journal	August 2016
MicroRNA-200c modulates epithelial-to-mesenchymal transition (EMT) in human colorectal cancer metastasis Hur, Keun; Toiyama, Yuji; Takahashi, Masanobu Gut, Vol. 62, Issue 9 https://doi.org/10.1136/gutjnl-2011-301846	journal	June 2012
Post-transcriptional regulatory network of epithelial-to-mesenchymal and mesenchymal-to-epithelial transitions Guo, Fei; Parker Kerrigan, Brittany C.; Yang, Da Journal of Hematology & Oncology, Vol. 7, Issue 1 https://doi.org/10.1186/1756-8722-7-19	journal	January 2014
An improved sequencing-based strategy to estimate locus-specific DNA methylation Brisotto, Giulia; di Gennaro, Alessandra; Damiano, Valentina BMC Cancer, Vol. 15, Issue 1 https://doi.org/10.1186/s12885-015-1646-6	journal	September 2015
Overexpression of the miR-141/200c cluster promotes the migratory and invasive ability of triple-negative breast cancer cells through the activation of the FAK and PI3K/AKT signaling pathways by secreting VEGF-A Choi, Sul Ki; Kim, Hoe Suk; Jin, Tiefeng BMC Cancer, Vol. 16, Issue 1 https://doi.org/10.1186/s12885-016-2620-7	journal	August 2016
Tamoxifen reverses epithelial–mesenchymal transition by demethylating miR-200c in triple-negative breast cancer cells Wang, Qian; Cheng, Yu; Wang, Yan BMC Cancer, Vol. 17, Issue 1 https://doi.org/10.1186/s12885-017-3457-4	journal	July 2017
DNA Methyltransferase Controls Stem Cell Aging by Regulating BMI1 and EZH2 through MicroRNAs So, Ah-Young; Jung, Ji-Won; Lee, Seunghee PLoS ONE, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pone.0019503	journal	May 2011
MicroRNA Alterations and Associated Aberrant DNA Methylation Patterns across Multiple Sample Types in Oral Squamous Cell Carcinoma Wiklund, Erik D.; Gao, Shan; Hulf, Toby PLoS ONE, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pone.0027840	journal	November 2011
MicroRNA Expression Characterizes Oligometastasis(es) Lussier, Yves A.; Xing, H. Rosie; Salama, Joseph K. PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0028650	journal	December 2011
MicroRNA-200 Family Modulation in Distinct Breast Cancer Phenotypes Castilla, María Ángeles; Díaz-Martín, Juan; Sarrió, David PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0047709	journal	October 2012
miRNA Gene Promoters Are Frequent Targets of Aberrant DNA Methylation in Human Breast Cancer Vrba, Lukas; Muñoz-Rodríguez, José L.; Stampfer, Martha R. PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0054398	journal	January 2013
miR-200b Inhibits Prostate Cancer EMT, Growth and Metastasis Williams, LaTanya V.; Veliceasa, Dorina; Vinokour, Elena PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0083991	journal	December 2013
Differential microRNA expression in breast cancer with different onset age Tsai, Hsiu-Pei; Huang, Shiang-Fu; Li, Chien-Fan PLOS ONE, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pone.0191195	journal	January 2018
MicroRNAs that affect prostate cancer: emphasis on prostate cancer in African Americans Jones, J.; Grizzle, W.; Wang, H. Biotechnic & Histochemistry, Vol. 88, Issue 7 https://doi.org/10.3109/10520295.2013.807069	journal	July 2013
Identification and Characterization of MicroRNAs Associated with Somatic Copy Number Alterations in Cancer Soh, Jihee; Cho, Hyejin; Choi, Chan-Hun Cancers, Vol. 10, Issue 12 https://doi.org/10.3390/cancers10120475	journal	November 2018
MicroRNAs as Mediators of the Ageing Process Harries, Lorna Genes, Vol. 5, Issue 3 https://doi.org/10.3390/genes5030656	journal	August 2014
Characterization of DNA Methylation in Circulating Tumor Cells Pixberg, Constantin; Schulz, Wolfgang; Stoecklein, Nikolas Genes, Vol. 6, Issue 4 https://doi.org/10.3390/genes6041053	journal	October 2015
TP53/MicroRNA Interplay in Hepatocellular Carcinoma Pollutri, Daniela; Gramantieri, Laura; Bolondi, Luigi International Journal of Molecular Sciences, Vol. 17, Issue 12 https://doi.org/10.3390/ijms17122029	journal	December 2016
A Circulating MicroRNA Signature as a Biomarker for Prostate Cancer in a High Risk Group Kelly, Brian; Miller, Nicola; Sweeney, Karl Journal of Clinical Medicine, Vol. 4, Issue 7 https://doi.org/10.3390/jcm4071369	journal	July 2015
MiR200 and miR302: Two Big Families Influencing Stem Cell Behavior Balzano, Francesca; Cruciani, Sara; Basoli, Valentina Molecules, Vol. 23, Issue 2 https://doi.org/10.3390/molecules23020282	journal	January 2018
miR-888 is an expressed prostatic secretions-derived microRNA that promotes prostate cell growth and migration Lewis, Holly; Lance, Raymond; Troyer, Dean Cell Cycle, Vol. 13, Issue 2 https://doi.org/10.4161/cc.26984	journal	November 2013
DNA methylation biomarkers discovered in silico detect cancer in liquid biopsies from non-small cell lung cancer patients Vrba, Lukas; Oshiro, Marc M.; Kim, Samuel S. Taylor & Francis https://doi.org/10.6084/m9.figshare.11294426.v1	text	January 2019

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