Epigenetic remodeling regulates transcriptional changes between ovarian cancer and benign precursors

JCI Insight

Volumn 1, Issue 13, 2016, Pages

  Elias, Kevin M ^a,b,c   Emori, Megan M ^a,d   Westerling, Thomas ^a   Long, Henry ^a   Budina Kolomets, Anna ^e   Li, Fugen ^a   MacDuffie, Emily ^a   Davis, Michelle R ^a,b,c   Holman, Alexander ^f   Lawney, Brian ^f   Freedman, Matthew L ^a   Quackenbush, John ^f   Brown, Myles ^a   Drapkin, Ronny ^a,c,e  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HARVARD UNIVERSITY   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85063024671     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.87988     Document Type: Article

References (50)

1. Carroll JS, et al. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell. 2005;122(1):33–43.
2. Shchuka VM, et al. Chromatin Dynamics in Lineage Commitment and Cellular Reprogramming. Genes (Basel). 2015;6(3):641–661.
3. Li J, et al. YY1 regulates melanocyte development and function by cooperating with MITF. PLoS Genet. 2012;8(5):e1002688
4. Laurette P, et al. Transcription factor MITF and remodeller BRG1 define chromatin organisation at regulatory elements in melanoma cells. Elife. 2015;4.
5. Chi P, et al. ETV1 is a lineage survival factor that cooperates with KIT in gastrointestinal stromal tumours. Nature. 2010;467(7317):849–853.
6. McGill GG, et al. Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell. 2002;109(6):707–718.
7. West JA, et al. A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature. 2009;460(7257):909–913.
8. Laury AR, et al. A comprehensive analysis of PAX8 expression in human epithelial tumors. Am J Surg Pathol. 2011;35(6):816–826.
9. Laury AR, et al. PAX8 reliably distinguishes ovarian serous tumors from malignant mesothelioma. Am J Surg Pathol. 2010;34(5):627–635.
10. Mittag J, Winterhager E, Bauer K, Grümmer R. Congenital hypothyroid female pax8-deficient mice are infertile despite thyroid hormone replacement therapy. Endocrinology. 2007;148(2):719–725.
11. Tone AA, et al. The role of the fallopian tube in ovarian cancer. Clin Adv Hematol Oncol. 2012;10(5):296–306.
12. Roh MH, Kindelberger D, Crum CP. Serous tubal intraepithelial carcinoma and the dominant ovarian mass: clues to serous tumor origin?. Am J Surg Pathol. 2009;33(3):376–383.
13. Perets R, Drapkin R. It’s Totally Tubular....Riding The New Wave of Ovarian Cancer Research. Cancer Res. 2016;76(1):10–17.
14. Jones PM, Drapkin R. Modeling High-Grade Serous Carcinoma: How Converging Insights into Pathogenesis and Genetics are Driving Better Experimental Platforms. Front Oncol. 2013;3:217.
15. Karst AM, Levanon K, Drapkin R. Modeling high-grade serous ovarian carcinogenesis from the fallopian tube. Proc Natl Acad Sci U S A. 2011;108(18):7547–7552.
16. Levanon K, et al. Primary ex vivo cultures of human fallopian tube epithelium as a model for serous ovarian carcinogenesis. Oncogene. 2010;29(8):1103–1113.
17. Perets R, et al. Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in Brca;Tp53;Pten models. Cancer Cell. 2013;24(6):751–765.
18. Elias KM, et al. Beyond genomics: critical evaluation of cell line utility for ovarian cancer research. Gynecol Oncol. 2015;139(1):97–103.
19. Domcke S, Sinha R, Levine DA, Sander C, Schultz N. Evaluating cell lines as tumour models by comparison of genomic profiles. Nat Commun. 2013;4:2126.
20. Anglesio MS, et al. Type-specific cell line models for type-specific ovarian cancer research. PLoS One. 2013;8(9):e72162.
21. Mitra AK, et al. In vivo tumor growth of high-grade serous ovarian cancer cell lines. Gynecol Oncol. 2015;138(2):372–377.
22. Hua G, et al. YAP induces high-grade serous carcinoma in fallopian tube secretory epithelial cells. Oncogene. 2016;35(17):2247–2265.
23. Karst AM, Drapkin R. Primary culture and immortalization of human fallopian tube secretory epithelial cells. Nat Protoc. 2012;7(9):1755–1764.
24. Cheung HW, et al. Systematic investigation of genetic vulnerabilities across cancer cell lines reveals lineage-specific dependencies in ovarian cancer. Proc Natl Acad Sci U S A. 2011;108(30):12372–12377.
25. Liu T, et al. Cistrome: an integrative platform for transcriptional regulation studies. Genome Biol. 2011;12(8):R83.
26. De Leo R, Miccadei S, Zammarchi E, Civitareale D. Role for p300 in Pax 8 induction of thyroperoxidase gene expression. J Biol Chem. 2000;275(44):34100–34105.
27. Bopp D, Burri M, Baumgartner S, Frigerio G, Noll M. Conservation of a large protein domain in the segmentation gene paired and in functionally related genes of Drosophila. Cell. 1986;47(6):1033–1040.
28. Frigerio G, Burri M, Bopp D, Baumgartner S, Noll M. Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network. Cell. 1986;47(5):735–746.
29. Mansouri A, Goudreau G, Gruss P. Pax genes and their role in organogenesis. Cancer Res. 1999;59(7 Suppl):1707s–1709s; discussion 1709s.
30. Chalepakis G, Fritsch R, Fickenscher H, Deutsch U, Goulding M, Gruss P. The molecular basis of the undulated/Pax-1 mutation. Cell. 1991;66(5):873–884.
31. Czerny T, Schaffner G, Busslinger M. DNA sequence recognition by Pax proteins: bipartite structure of the paired domain and its binding site. Genes Dev. 1993;7(10):2048–2061.
32. Mansouri A, Hallonet M, Gruss P. Pax genes and their roles in cell differentiation and development. Curr Opin Cell Biol. 1996;8(6):851–857.
33. Di Palma T, Lucci V, de Cristofaro T, Filippone MG, Zannini M. A role for PAX8 in the tumorigenic phenotype of ovarian cancer cells. BMC Cancer. 2014;14:292.
34. Ruiz-Llorente S, et al. Genome-wide analysis of Pax8 binding provides new insights into thyroid functions. BMC Genomics. 2012;13:147.
35. Clauss A, et al. Overexpression of elafin in ovarian carcinoma is driven by genomic gains and activation of the nuclear factor kappaB pathway and is associated with poor overall survival. Neoplasia. 2010;12(2):161–172.
36. Labidi-Galy SI, et al. Elafin drives poor outcome in high-grade serous ovarian cancers and basal-like breast tumors. Oncogene. 2015;34(3):373–383.
37. Drapkin R, et al. Human epididymis protein 4 (HE4) is a secreted glycoprotein that is overexpressed by serous and endometrioid ovarian carcinomas. Cancer Res. 2005;65(6):2162–2169.
38. Flesken-Nikitin A, Hwang CI, Cheng CY, Michurina TV, Enikolopov G, Nikitin AY. Ovarian surface epithelium at the junction area contains a cancer-prone stem cell niche. Nature. 2013;495(7440):241–245.
39. Sun Y, Jia X, Wu X. High Expressions of Lgr5 and ALDH1 in Primary Epithelial Ovarian Cancer Correlate with Advanced Tumor Stage and Grade as well as Poor Prognosis of the Patients [published online ahead of print June 20, 2015]. Gynecol Obstet Invest. doi: 10.1159/000431222.
40. Ren Y, et al. Targeted tumor-penetrating siRNA nanocomplexes for credentialing the ovarian cancer oncogene ID4. Sci Transl Med. 2012;4(147):147ra112.
41. Kountourakis P, et al. Expression and prognostic significance of kallikrein-related peptidase 8 protein levels in advanced ovarian cancer by using automated quantitative analysis. Thromb Haemost. 2009;101(3):541–546.
42. Magklara A, et al. The human KLK8 (neuropsin/ovasin) gene: identification of two novel splice variants and its prognostic value in ovarian cancer. Clin Cancer Res. 2001;7(4):806–811.
43. Zhang X, et al. Identification of focally amplified lineage-specific super-enhancers in human epithelial cancers. Nat Genet. 2016;48(2):176–182.
44. Hansen CG, Moroishi T, Guan KL. YAP and TAZ: a nexus for Hippo signaling and beyond. Trends Cell Biol. 2015;25(9):499–513.
45. Jolma A, et al. DNA-dependent formation of transcription factor pairs alters their binding specificity. Nature. 2015;527(7578):384–388.
46. Zanconato F, et al. Genome-wide association between YAP/TAZ/TEAD and AP-1 at enhancers drives oncogenic growth. Nat Cell Biol. 2015;17(9):1218–1227.
47. Stein C, et al. YAP1 Exerts Its Transcriptional Control via TEAD-Mediated Activation of Enhancers. PLoS Genet. 2015;11(8):e1005465.
48. Cejas P, et al. Chromatin immunoprecipitation from fixed clinical tissues reveals tumor-specific enhancer profiles. Nat Med. 2016;22(6):685–691.
49. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11(10):R106.
50. Trapnell C, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7(3):562–578.