Multivalent epigenetic marks confer microenvironment-responsive epigenetic plasticity to ovarian cancer cells

References

• Campos EI, Reinberg D. Histones: annotating chromatin. Annu Rev Genet 2009; 43:559 - 599
   PubMed Web of Science ®Google Scholar
• Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 2008; 9:465 - 476
   PubMed Web of Science ®Google Scholar
• Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293:1074 - 1080
   PubMed Web of Science ®Google Scholar
• Esteller M. Epigenetics in cancer. N Engl J Med 2008; 358:1148 - 1159
   PubMed Web of Science ®Google Scholar
• Rice JC, Allis CD. Code of silence. Nature 2001; 414:258 - 261
   PubMed Web of Science ®Google Scholar
• Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006; 125:315 - 326
   PubMed Web of Science ®Google Scholar
• Weishaupt H, Sigvardsson M, Attema JL. Epigenetic chromatin states uniquely define the developmental plasticity of murine hematopoietic stem cells. Blood 2010; 115:247 - 256
   PubMedGoogle Scholar
• Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 2006; 20:1123 - 1136
   PubMed Web of Science ®Google Scholar
• Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007; 447:425 - 432
   PubMed Web of Science ®Google Scholar
• Rodriguez J, Munoz M, Vives L, Frangou CG, Groudine M, Peinado MA. Bivalent domains enforce transcriptional memory of DNA methylated genes in cancer cells. Proc Natl Acad Sci USA 2008; 105:19809 - 19814
   PubMed Web of Science ®Google Scholar
• McGarvey KM, Van Neste L, Cope L, Ohm JE, Herman JG, Van Criekinge W, et al. Defining a chromatin pattern that characterizes DNA-hypermethylated genes in colon cancer cells. Cancer Res 2008; 68:5753 - 5759
   Google Scholar
• Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 2007; 39:232 - 236
   PubMed Web of Science ®Google Scholar
• Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C, et al. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet 2008; 40:741 - 750
   PubMed Web of Science ®Google Scholar
• Sparmann A, van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 2006; 6:846 - 856
   PubMed Web of Science ®Google Scholar
• Wernig M, Lengner CJ, Hanna J, Lodato MA, Steine E, Foreman R, et al. A drug-inducible transgenic system for direct reprogramming of multiple somatic cell types. Nat Biotechnol 2008; 26:916 - 924
   PubMed Web of Science ®Google Scholar
• Hochedlinger K, Plath K. Epigenetic reprogramming and induced pluripotency. Development 2009; 136:509 - 523
   PubMed Web of Science ®Google Scholar
• Graf T, Enver T. Forcing cells to change lineages. Nature 2009; 462:587 - 594
   PubMed Web of Science ®Google Scholar
• Dalerba P, Cho RW, Clarke MF. Cancer stem cells: models and concepts. Annu Rev Med 2007; 58:267 - 284
   PubMed Web of Science ®Google Scholar
• Jordan CT. Cancer stem cells: controversial or just misunderstood?. Cell Stem Cell 2009; 4:203 - 205
   PubMed Web of Science ®Google Scholar
• Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009; 9:265 - 273
   PubMed Web of Science ®Google Scholar
• Papageorgis P, Lambert AW, Ozturk S, Gao F, Pan H, Manne U, et al. Smad signaling is required to maintain epigenetic silencing during breast cancer progression. Cancer Res 2010; 70:968 - 978
   Google Scholar
• Postovit LM, Margaryan NV, Seftor EA, Kirschmann DA, Lipavsky A, Wheaton WW, et al. Human embryonic stem cell microenvironment suppresses the tumorigenic phenotype of aggressive cancer cells. Proc Natl Acad Sci USA 2008; 105:4329 - 4334
   PubMed Web of Science ®Google Scholar
• Hendrix MJ, Seftor EA, Seftor RE, Kasemeier-Kulesa J, Kulesa PM, Postovit LM. Reprogramming metastatic tumour cells with embryonic microenvironments. Nat Rev Cancer 2007; 7:246 - 255
   PubMed Web of Science ®Google Scholar
• Bhowmick NA, Neilson EG, Moses HL. Stromal fibroblasts in cancer initiation and progression. Nature 2004; 432:332 - 337
   PubMed Web of Science ®Google Scholar
• Bissell MJ, Labarge MA. Context, tissue plasticity and cancer: are tumor stem cells also regulated by the microenvironment?. Cancer Cell 2005; 7:17 - 23
   PubMed Web of Science ®Google Scholar
• Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 2007; 39:237 - 242
   PubMed Web of Science ®Google Scholar
• Ke XS, Qu Y, Rostad K, Li WC, Lin B, Halvorsen OJ, et al. Genome-wide profiling of histone h3 lysine 4 and lysine 27 trimethylation reveals an epigenetic signature in prostate carcinogenesis. PLoS One 2009; 4:4687
   PubMed Web of Science ®Google Scholar
• Shield K, Ackland ML, Ahmed N, Rice GE. Multicellular spheroids in ovarian cancer metastases: Biology and pathology. Gynecol Oncol 2009; 113:143 - 148
   PubMed Web of Science ®Google Scholar
• L'Esperance S, Bachvarova M, Tetu B, Mes-Masson AM, Bachvarov D. Global gene expression analysis of early response to chemotherapy treatment in ovarian cancer spheroids. BMC Genomics 2008; 9:99
   PubMed Web of Science ®Google Scholar
• Jin VX, Rabinovich A, Squazzo SL, Green R, Farnham PJ. A computational genomics approach to identify cis-regulatory modules from chromatin immunoprecipitation microarray data—a case study using E2F1. Genome Res 2006; 16:1585 - 1595
   PubMed Web of Science ®Google Scholar
• Balch C, Nephew KP, Huang TH, Bapat SA. Epigenetic “bivalently marked” process of cancer stem cell-driven tumorigenesis. Bioessays 2007; 29:842 - 845
   PubMed Web of Science ®Google Scholar
• Feinberg AP. Phenotypic plasticity and the epigenetics of human disease. Nature 2007; 447:433 - 440
   PubMed Web of Science ®Google Scholar
• Ekins S, Nikolsky Y, Bugrim A, Kirillov E, Nikolskaya T. Pathway mapping tools for analysis of high content data. Methods Mol Biol 2007; 356:319 - 350
   PubMedGoogle Scholar
• Tsuda N, Kawano K, Efferson CL, Ioannides CG. Synthetic microRNA and double-stranded RNA targeting the 3′-untranslated region of HER-2/neu mRNA inhibit HER-2 protein expression in ovarian cancer cells. Int J Oncol 2005; 27:1299 - 1306
   PubMed Web of Science ®Google Scholar
• Zhang L, Huang J, Yang N, Greshock J, Megraw MS, Giannakakis A, et al. microRNAs exhibit high frequency genomic alterations in human cancer. Proc Natl Acad Sci USA 2006; 103:9136 - 9141
   PubMed Web of Science ®Google Scholar
• Shell S, Park SM, Radjabi AR, Schickel R, Kistner EO, Jewell DA, et al. Let-7 expression defines two differentiation stages of cancer. Proc Natl Acad Sci USA 2007; 104:11400 - 11405
   PubMed Web of Science ®Google Scholar
• Giannakakis A, Coukos G, Hatzigeorgiou A, Sandaltzopoulos R, Zhang L. miRNA genetic alterations in human cancers. Expert Opin Biol Ther 2007; 7:1375 - 1386
   PubMed Web of Science ®Google Scholar
• Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, Nikitin AY. MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res 2007; 67:8433 - 8438
   PubMed Web of Science ®Google Scholar
• Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, et al. MicroRNA signatures in human ovarian cancer. Cancer Res 2007; 67:8699 - 8707
   PubMed Web of Science ®Google Scholar
• Gillis AJ, Stoop HJ, Hersmus R, Oosterhuis JW, Sun Y, Chen C, et al. High-throughput microRNAome analysis in human germ cell tumours. J Pathol 2007; 213:319 - 328
   PubMed Web of Science ®Google Scholar
• Corney DC, Nikitin AY. MicroRNA and ovarian cancer. Histol Histopathol 2008; 23:1161 - 1169
   PubMed Web of Science ®Google Scholar
• Pan G, Tian S, Nie J, Yang C, Ruotti V, Wei H, et al. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 2007; 1:299 - 312
   PubMed Web of Science ®Google Scholar
• Abbosh PH, Montgomery JS, Starkey JA, Novotny M, Zuhowski EG, Egorin MJ, et al. Dominant-negative histone H3 lysine 27 mutant derepresses silenced tumor suppressor genes and reverses the drug-resistant phenotype in cancer cells. Cancer Res 2006; 66:5582 - 5591
   PubMed Web of Science ®Google Scholar
• Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10:593 - 601
   PubMed Web of Science ®Google Scholar
• Korpal M, Lee ES, Hu G, Kang Y. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 2008; 283:14910 - 14914
   PubMed Web of Science ®Google Scholar
• Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133:704 - 715
   PubMed Web of Science ®Google Scholar
• Kudo-Saito C, Shirako H, Takeuchi T, Kawakami Y. Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell 2009; 15:195 - 206
   PubMed Web of Science ®Google Scholar
• Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006; 441:349 - 353
   PubMed Web of Science ®Google Scholar
• Kleer CG, Cao Q, Varambally S, Shen R, Ota I, Tomlins SA, et al. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci USA 2003; 100:11606 - 11611
   PubMed Web of Science ®Google Scholar
• Bryant RJ, Cross NA, Eaton CL, Hamdy FC, Cunliffe VT. EZH2 promotes proliferation and invasiveness of prostate cancer cells. Prostate 2007; 67:547 - 556
   PubMed Web of Science ®Google Scholar
• Bapat SA, Mali AM, Koppikar CB, Kurrey NK. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 2005; 65:3025 - 3029
   PubMed Web of Science ®Google Scholar
• Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 2008; 68:4311 - 4320
   PubMed Web of Science ®Google Scholar
• Schuebel KE, Chen W, Cope L, Glockner SC, Suzuki H, Yi JM, et al. Comparing the DNA hypermethylome with gene mutations in human colorectal cancer. PLoS Genet 2007; 3:1709 - 1723
   PubMed Web of Science ®Google Scholar
• Dreesen O, Brivanlou AH. Signaling pathways in cancer and embryonic stem cells. Stem Cell Rev 2007; 3:7 - 17
   PubMed Web of Science ®Google Scholar
• Moss NM, Barbolina MV, Liu Y, Sun L, Munshi HG, Stack MS. Ovarian cancer cell detachment and multicellular aggregate formation are regulated by membrane type 1 matrix metalloproteinase: a potential role in I.p. metastatic dissemination. Cancer Res 2009; 69:7121 - 7129
   PubMed Web of Science ®Google Scholar
• Maherali N, Sridharan R, Xie W, Utikal J, Eminli S, Arnold K, et al. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 2007; 1:55 - 70
   PubMed Web of Science ®Google Scholar
• Huangfu D, Osafune K, Maehr R, Guo W, Eijkelenboom A, Chen S, et al. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 2008; 26:1269 - 1275
   PubMed Web of Science ®Google Scholar
• Shen CN, Slack JM, Tosh D. Molecular basis of transdifferentiation of pancreas to liver. Nat Cell Biol 2000; 2:879 - 887
   PubMed Web of Science ®Google Scholar
• Morroni M, Giordano A, Zingaretti MC, Boiani R, De Matteis R, Kahn BB, et al. Reversible transdifferentiation of secretory epithelial cells into adipocytes in the mammary gland. Proc Natl Acad Sci USA 2004; 101:16801 - 16806
   PubMed Web of Science ®Google Scholar
• Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB, et al. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 2008; 30:755 - 766
   PubMed Web of Science ®Google Scholar
• Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007; 128:683 - 692
   PubMed Web of Science ®Google Scholar
• Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: biology, endocrinology and pathology. Endocr Rev 2001; 22:255 - 288
   PubMed Web of Science ®Google Scholar
• Liao MJ, Zhang CC, Zhou B, Zimonjic DB, Mani SA, Kaba M, et al. Enrichment of a population of mammary gland cells that form mammospheres and have in vivo repopulating activity. Cancer Res 2007; 67:8131 - 8138
   PubMed Web of Science ®Google Scholar
• Golmohammadi MG, Blackmore DG, Large B, Azari H, Esfandiary E, Paxinos G, et al. Comparative analysis of the frequency and distribution of stem and progenitor cells in the adult mouse brain. Stem Cells 2008; 26:979 - 987
   PubMed Web of Science ®Google Scholar
• Cicero SA, Johnson D, Reyntjens S, Frase S, Connell S, Chow LM, et al. Cells previously identified as retinal stem cells are pigmented ciliary epithelial cells. Proc Natl Acad Sci USA 2009; 106:6685 - 6690
   PubMed Web of Science ®Google Scholar
• Li L, Fukunaga-Kalabis M, Yu H, Xu X, Kong J, Lee JT, et al. Human dermal stem cells differentiate into functional epidermal melanocytes. J Cell Sci 2010; 123:853 - 860
   PubMed Web of Science ®Google Scholar
• Suva ML, Riggi N, Janiszewska M, Radovanovic I, Provero P, Stehle JC, et al. EZH2 is essential for glioblastoma cancer stem cell maintenance. Cancer Res 2009; 69:9211 - 9218
   PubMed Web of Science ®Google Scholar
• Ahmed N, Thompson EW, Quinn MA. Epithelial-mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: an exception to the norm. J Cell Physiol 2007; 213:581 - 588
   PubMed Web of Science ®Google Scholar
• Bendoraite A, Knouf EC, Garg KS, Parkin RK, Kroh EM, O'Briant KC, et al. Regulation of miR-200 family microRNAs and ZEB transcription factors in ovarian cancer: evidence supporting a mesothelial-to-epithelial transition. Gynecol Oncol 2010; 116:117 - 125
   PubMed Web of Science ®Google Scholar
• Kusumbe AP, Mali AM, Bapat SA. CD133-expressing stem cells associated with ovarian metastases establish an endothelial hierarchy and contribute to tumor vasculature. Stem Cells 2009; 27:498 - 508
   PubMed Web of Science ®Google Scholar
• Sood AK, Seftor EA, Fletcher MS, Gardner LM, Heidger PM, Buller RE, et al. Molecular determinants of ovarian cancer plasticity. Am J Pathol 2001; 158:1279 - 1288
   PubMed Web of Science ®Google Scholar
• Hudson LG, Zeineldin R, Stack MS. Phenotypic plasticity of neoplastic ovarian epithelium: unique cadherin profiles in tumor progression. Clin Exp Metastasis 2008; 25:643 - 655
   PubMed Web of Science ®Google Scholar
• Katz E, Skorecki K, Tzukerman M. Niche-dependent tumorigenic capacity of malignant ovarian ascitesderived cancer cell subpopulations. Clin Cancer Res 2009; 15:70 - 80
   PubMed Web of Science ®Google Scholar
• Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008; 134:521 - 533
   PubMed Web of Science ®Google Scholar
• Szotek PP, Pieretti-Vanmarcke R, Masiakos PT, Dinulescu DM, Connolly D, Foster R, et al. Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc Natl Acad Sci USA 2006; 103:11154 - 11159
   PubMed Web of Science ®Google Scholar
• Ahluwalia A, Hurteau JA, Bigsby RM, Nephew KP. DNA methylation in ovarian cancer. II. Expression of DNA methyltransferases in ovarian cancer cell lines and normal ovarian epithelial cells. Gynecol Oncol 2001; 82:299 - 304
   PubMed Web of Science ®Google Scholar
• Qin H, Chan MW, Liyanarachchi S, Balch C, Potter D, Souriraj IJ, et al. An integrative ChIP-chip and gene expression profiling to model SMAD regulatory modules. BMC Syst Biol 2009; 3:73
   PubMed Web of Science ®Google Scholar
• Fan M, Yan PS, Hartman-Frey C, Chen L, Paik H, Oyer SL, et al. Diverse gene expression and DNA methylation profiles correlate with differential adaptation of breast cancer cells to the antiestrogens tamoxifen and fulvestrant. Cancer Res 2006; 66:11954 - 11966
   Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402 - 408
   PubMed Web of Science ®Google Scholar
• Li M, Balch C, Montgomery JS, Jeong M, Chung JH, Yan P, et al. Integrated analysis of DNA methylation and gene expression reveals specific signaling pathways associated with platinum resistance in ovarian cancer. BMC Med Genomics 2009; 2:34
   PubMed Web of Science ®Google Scholar
• Nam S, Li M, Choi K, Balch C, Kim S, Nephew KP. MicroRNA and mRNA integrated analysis (MMIA): a web tool for examining biological functions of microRNA expression. Nucleic Acids Res 2009; 37:356 - 362
   Web of Science ®Google Scholar
• Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102:15545 - 15550
   PubMed Web of Science ®Google Scholar
• Xin F, Li M, Balch C, Thomson M, Fan M, Liu Y, et al. Computational analysis of microRNA profiles and their target genes suggests significant involvement in breast cancer antiestrogen resistance. Bioinformatics 2009; 25:430 - 434
   PubMed Web of Science ®Google Scholar
• Thomson JM, Parker J, Perou CM, Hammond SM. A custom microarray platform for analysis of microRNA gene expression. Nat Methods 2004; 1:47 - 53
   PubMed Web of Science ®Google Scholar
• Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998; 95:14863 - 14868
   PubMed Web of Science ®Google Scholar