Matrix stiffness induces a tumorigenic phenotype in mammary epithelium through changes in chromatin accessibility (original) (raw)

• Levental, K. R. et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891–906 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Provenzano, P. P., Inman, D. R., Eliceiri, K. W. & Keely, P. J. Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK–ERK linkage. Oncogene 28, 4326–4343 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Choquet, D., Felsenfeld, D. P. & Sheetz, M. P. Extracellular matrix rigidity causes strengthening of integrin–cytoskeleton linkages. Cell 88, 39–48 (1997).
  Article CAS PubMed Google Scholar
• Paszek, M. J. et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241–254 (2005).
  Article CAS PubMed Google Scholar
• Del Rio, A. et al. Stretching single talin rod molecules activates vinculin binding. Science 323, 638–641 (2009).
  Article CAS PubMed Google Scholar
• Elosegui-Artola, A. et al. Mechanical regulation of a molecular clutch defines force transmission and transduction in response to matrix rigidity. Nat. Cell Biol. 18, 540–548 (2016).
  Article CAS PubMed Google Scholar
• Aragona, M. et al. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154, 1047–1059 (2013).
  Article CAS PubMed Google Scholar
• Chaudhuri, O. et al. Extracellular matrix stiffness and composition jointly regulate the induction of malignant phenotypes in mammary epithelium. Nat. Mater. 13, 970–978 (2014).
  Article CAS PubMed Google Scholar
• Uhler, C. & Shivashankar, G. V. Regulation of genome organization and gene expression by nuclear mechanotransduction. Nat. Rev. Mol. Cell Biol. 18, 717–727 (2017).
  Article CAS PubMed Google Scholar
• Maniatis, T., Goodbourn, S. & Fischer, J. A. Regulation of inducible and tissue-specific gene expression. Science 236, 1237–1245 (1987).
  Article CAS PubMed Google Scholar
• Pique-Regi, R. et al. Accurate inference of transcription factor binding from DNA sequence and chromatin accessibility data. Genome Res. 21, 447–455 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Kouzarides, T. Chromatin modifications and their function. Cell 128, 693–705 (2007).
  Article CAS PubMed Google Scholar
• Swift, J. et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 1240104 (2013).
  Article PubMed PubMed Central CAS Google Scholar
• Jain, N., Iyer, K. V., Kumar, A. & Shivashankar, G. V. Cell geometric constraints induce modular gene-expression patterns via redistibution of HDAC3 regulated by actomyosin contractility. Proc. Natl Acad. Sci. USA 110, 11349–11354 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Li, Y., Tang, C. B. & Kilian, K. A. Matrix mechanics influence fibroblast–myofibroblast transition by directing the localization of histone deacetylase 4. Cell. Mol. Bioeng. 10, 405–415 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Flavahan, W. A., Gaskell, E. & Bernstein, B. E. Epigenetic plasticity and the hallmarks of cancer. Science 357, eaal2380 (2017).
  Article PubMed PubMed Central CAS Google Scholar
• McDonald, O. G., Wu, H., Timp, W., Doi, A. & Feinberg, A. P. Genome-scale epigenetic reprogramming during epithelial-to-mesenchymal transition. Nat. Struct. Mol. Biol. 18, 867–874 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Tajik, A. et al. Transcription upregulation via force-induced direct stretching of chromatin. Nat. Mater. 15, 1287–1296 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Gallo, M. et al. MLL5 orchestrates a cancer self-renewal state by repressing the histone variant H3.3 and globally reorganizing chromatin. Cancer Cell 28, 715–729 (2015).
  Article CAS PubMed Google Scholar
• Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Ooi, J. Y. et al. HDAC inhibition attenuates cardiac hypertrophy by acetylation and deacetylation of target genes. Epigenetics 10, 418–430 (2015).
  Article PubMed PubMed Central Google Scholar
• Rafehi, H. et al. Systems approach to the pharmacological actions of HDAC inhibitors reveals EP300 activities and convergent mechanisms of regulation in diabetes. Epigenetics 12, 991–1003 (2017).
  Article PubMed PubMed Central Google Scholar
• Fork, C. et al. Epigenetic control of microsomal prostaglandin E synthase-1 by HDAC-mediated recruitment of p300. J. Lipid Res. 58, 386–392 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Rafehi, H. et al. Vascular histone deacetylation by pharmacological HDAC inhibition. Genome Res. 24, 1271–1284 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Rafehi, H. & El-Osta, A. HDAC inhibition in vascular endothelial cells regulates the expression of ncRNAs. Noncoding RNA 2, 4 (2016).
  PubMed Central Google Scholar
• Chen, F. et al. Inhibition of histone deacetylase reduces transcription of NADPH oxidases and ROS production and ameliorates pulmonary arterial hypertension. Free Radic. Biol. Med 99, 167–178 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Qu, K. et al. Chromatin accessibility landscape of cutaneous T cell lymphoma and dynamic response to HDAC inhibitors. Cancer Cell 32, 27–41 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Kaczynski, J., Cook, T. & Urrutia, R. Sp1- and Kruppel-like transcription factors. Genome Biol. 4, 1–8 (2003).
  Article Google Scholar
• Han, H. et al. TRRUSTv2: an expanded reference database of human and mouse transcriptional regulatory interactions. Nucleic Acids Res. 46, D380–D386 (2018).
  Article CAS PubMed Google Scholar
• Hsu, M. C., Chang, H. C. & Hung, W. C. HER-2/neu represses the metastasis suppressor RECK via ERK and Sp transcription factors to promote cell invasion. J. Biol. Chem. 281, 4718–4725 (2006).
  Article CAS PubMed Google Scholar
• Stowers, R. S. et al. Extracellular matrix stiffening induces a malignant phenotypic transition in breast epithelial cells. Cell. Mol. Bioeng. 10, 114–123 (2016).
  Article PubMed PubMed Central CAS Google Scholar
• Zhang, Y., Liao, M. & Dufau, M. L. Phosphatidylinositol 3-kinase/protein kinase Cζ-induced phosphorylation of Sp1 and p107 repressor release have a critical role in histone deacetylase inhibitor-mediated derepression of transcription of the luteinizing hormone receptor gene. Mol. Cell Biol. 26, 6748–6761 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Doetzlhofer, A. et al. Histone deacetylase 1 can repress transcription by binding to Sp1. Mol. Cell Biol. 19, 5504–5511 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Liu, S. et al. Sp1/NFκB/HDAC/miR-29b regulatory network in KIT-driven myeloid leukemia. Cancer Cell 17, 333–347 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Petersen, O. W., Ronnov-Jessen, L., Howlett, A. R. & Bissell, M. J. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc. Natl Acad. Sci. USA 89, 9064–9068 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Uhlen, M. et al. Tissue-based map of the human proteome. Science 347, 1260419 (2015).
  Article PubMed CAS Google Scholar
• Heo, S. J. et al. Biophysical regulation of chromatin architecture instills a mechanical memory in mesenchymal stem cells. Sci. Rep. 5, 16895 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Jain, N., Iyer, K. V., Kumar, A. & Shivashankar, G. V. Cell geometric constraints induce modular gene-expression patterns via redistribution of HDAC3 regulated by actomyosin contractility. Proc. Natl Acad. Sci. USA 110, 11349–11354 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Demmerle, J., Koch, A. J. & Holaska, J. M. The nuclear envelope protein emerin binds directly to histone deacetylase 3 (HDAC3) and activates HDAC3 activity. J. Biol. Chem. 287, 22080–22088 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Le, H. Q. et al. Mechanical regulation of transcription controls Polycomb-mediated gene silencing during lineage commitment. Nat. Cell Biol. 18, 864–875 (2016).
  Article CAS PubMed Google Scholar
• Xu, R. et al. Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specific function. J. Cell Biol. 184, 57–66 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Le Beyec, J. et al. Cell shape regulates global histone acetylation in human mammary epithelial cells. Exp. Cell Res. 313, 3066–3075 (2007).
  Article PubMed PubMed Central CAS Google Scholar
• Fraga, M. F. et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat. Genet. 37, 391–400 (2005).
  Article CAS PubMed Google Scholar
• Bibikova, M. et al. Human embryonic stem cells have a unique epigenetic signature. Genome Res. 16, 1075–1083 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Wisdom, K. & Chaudhuri, O. 3D cell culture in interpenetrating networks of alginate and rBM matrix. Methods Mol. Biol. 1612, 29–37 (2017).
  Article CAS PubMed Google Scholar
• Thevenaz, P., Ruttimann, U. E. & Unser, M. A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 7, 27–41 (1998).
  Article CAS PubMed Google Scholar
• Thielicke, W. & Stamhuis, E. J. Towards user-friendly, affordable and accurate digital particle image velocimetry in MATLAB. J. Open Res. Softw. 2, e30 (2014).
  Article Google Scholar
• Debnath, J., Muthuswamy, S. K. & Brugge, J. S. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256–268 (2003).
  Article CAS PubMed Google Scholar
• Buenrostro, J. D., Wu, B., Chang, H. Y. & Greenleaf, W. J. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. 109, 21–29 (2015).
  Article PubMed PubMed Central Google Scholar
• Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
  Article PubMed PubMed Central CAS Google Scholar
• Machanick, P. & Bailey, T. L. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27, 1696–1697 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Szklarczyk, D. et al. STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 43, D447–D452 (2015).
  Article CAS PubMed Google Scholar
• ACTB: Tissue-breast (Human Protein Atlas, 2019); https://www.proteinatlas.org/ENSG00000075624-ACTB/tissue/breast#