Tissue-of-origin-specific gene repositioning in breast and prostate cancer
Tóm tắt
Genes have preferential non-random spatial positions within the cell nucleus. The nuclear position of a subset of genes differ between cell types and some genes undergo repositioning events in disease, including cancer. It is currently unclear whether the propensity of a gene to reposition reflects an intrinsic property of the locus or the tissue. Using quantitative FISH analysis of a set of genes which reposition in cancer, we test here the tissue specificity of gene repositioning in normal and malignant breast or prostate tissues. We find tissue-specific organization of the genome in normal breast and prostate with 40 % of genes occupying differential positions between the two tissue types. While we demonstrate limited overlap between gene sets that repositioned in breast and prostate cancer, we identify two genes that undergo disease-related gene repositioning in both cancer types. Our findings indicate that gene repositioning in cancer is tissue-of-origin specific.
Tài liệu tham khảo
Battulin N et al (2015) Comparison of the 3D organization of sperm and fibroblast genomes using the Hi-C approach. Genome Biol 16:77. doi:10.1186/s13059-015-0642-0
Borden J, Manuelidis L (1988) Movement of the X chromosome in epilepsy. Science 242:1687–1691
Boutanaev AM, Mikhaylova LM, Nurminsky DI (2005) The pattern of chromosome folding in interphase is outlined by the linear gene density profile. Mol Cell Biol 25:8379–8386
Boyle S, Gilchrist S, Bridger JM, Mahy NL, Ellis JA, Bickmore WA (2001) The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum Mol Genet 10:211–219
Cremer M et al (2003) Inheritance of gene density-related higher order chromatin arrangements in normal and tumor cell nuclei. J Cell Biol 162:809–820
Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA (1999) Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol 145:1119–1131
Ferrai C, de Castro IJ, Lavitas L, Chotalia M, Pombo A (2010) Gene positioning. Cold Spring Harbor Perspect Biol 2:a000588. doi:10.1101/cshperspect.a000588
Foster HA, Griffin DK, Bridger JM (2012) Interphase chromosome positioning in in vitro porcine cells and ex vivo porcine tissues. BMC Cell Biol 13:30. doi:10.1186/1471-2121-13-30
Guelen L et al (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:948–951. doi:10.1038/nature06947
Hiratani I et al (2008) Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol 6:e245. doi:10.1371/journal.pbio.0060245
Kosak ST, Skok JA, Medina KL, Riblet R, Le Beau MM, Fisher AG, Singh H (2002) Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science 296:158–162
Kurz A et al (1996) Active and inactive genes localize preferentially in the periphery of chromosome territories. J Cell Biol 135:1195–1205
Leshner M, Devine M, Roloff GW, True LD, Misteli T, Meaburn KJ (2015) Locus-specific gene repositioning in prostate cancer. Mol Biol Cell. doi:10.1091/mbc.E15-05-0280
Lieberman-Aiden E et al (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–293. doi:10.1126/science.1181369
Mahy NL, Perry PE, Gilchrist S, Baldock RA, Bickmore WA (2002) Spatial organization of active and inactive genes and noncoding DNA within chromosome territories. J Cell Biol 157:579–589
Mayer R, Brero A, von Hase J, Schroeder T, Cremer T, Dietzel S (2005) Common themes and cell type specific variations of higher order chromatin arrangements in the mouse. BMC Cell Biol 6:44
Meaburn KJ (2010) Fluorescence in situ hybridization on 3D cultures of tumor cells. Methods Mol Biol 659:323–336. doi:10.1007/978-1-60761-789-1_25
Meaburn KJ, Misteli T (2008) Locus-specific and activity-independent gene repositioning during early tumorigenesis. J Cell Biol 180:39–50
Meaburn KJ et al (2007) Primary laminopathy fibroblasts display altered genome organization and apoptosis. Aging cell 6:139–153. doi:10.1111/j.1474-9726.2007.00270.x
Meaburn KJ, Newbold RF, Bridger JM (2008) Positioning of human chromosomes in murine cell hybrids according to synteny. Chromosoma 117:579–591. doi:10.1007/s00412-008-0175-3
Meaburn KJ, Gudla PR, Khan S, Lockett SJ, Misteli T (2009) Disease-specific gene repositioning in breast cancer. J Cell Biol 187:801–812. doi:10.1083/jcb.200909127
Meaburn KJ, Burman B, Misteli T (2016) Spatial genome organization and disease. In: Dellaire G, Basett-Jones D (eds) The functional nucleus. Springer DE (in press)
Mehta IS, Eskiw CH, Arican HD, Kill IR, Bridger JM (2011) Farnesyltransferase inhibitor treatment restores chromosome territory positions and active chromosome dynamics in Hutchinson-Gilford progeria syndrome cells. Genome Biol 12:R74. doi:10.1186/gb-2011-12-8-r74
Mewborn SK et al (2010) Altered chromosomal positioning, compaction, and gene expression with a lamin A/C gene mutation. PLoS One 5:e14342. doi:10.1371/journal.pone.0014342
Mikelsaar R, Paves H, Org K, Mikelsaar AV (2014) Chromosome variant 1qh- and its influence on the 3D organization of chromosome 1 heterochromatin in interphase nucleus of patients with endometriosis. J Genet 93:219–223
Murata S et al (2007) Conservation and alteration of chromosome territory arrangements in thyroid carcinoma cell nuclei. Thyroid 17:489–496. doi:10.1089/thy.2006.0328
Parada L, McQueen P, Misteli T (2004) Tissue-specific spatial organization of genomes. Genome Biol 7:R44
Paz N et al (2015) Expression of the DYRK1A gene correlates with its 3D positioning in the interphase nucleus of Down syndrome cells. Chromosome Res. doi:10.1007/s10577-015-9467-7
Peric-Hupkes D et al (2010) Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell 38:603–613. doi:10.1016/j.molcel.2010.03.016
Risbridger GP, Davis ID, Birrell SN, Tilley WD (2010) Breast and prostate cancer: more similar than different. Nat Rev Cancer 10:205–212. doi:10.1038/nrc2795
Scheuermann MO, Tajbakhsh J, Kurz A, Saracoglu K, Eils R, Lichter P (2004) Topology of genes and nontranscribed sequences in human interphase nuclei. Exp Cell Res 301:266–279
Shopland LS et al (2006) Folding and organization of a contiguous chromosome region according to the gene distribution pattern in primary genomic sequence. J Cell Biol 174:27–38
Therizols P, Illingworth RS, Courilleau C, Boyle S, Wood AJ, Bickmore WA (2014) Chromatin decondensation is sufficient to alter nuclear organization in embryonic stem cells. Science 346:1238–1242. doi:10.1126/science.1259587
Timme S et al (2011) Nuclear position and shape deformation of chromosome 8 territories in pancreatic ductal adenocarcinoma. Anal Cell Pathol 34:21–33. doi:10.3233/ACP-2011-0004
Towbin BD et al (2012) Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150:934–947. doi:10.1016/j.cell.2012.06.051
Volpi EV et al (2000) Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J Cell Sci 113(Pt 9):1565–1576
Wiech T et al (2005) Human archival tissues provide a valuable source for the analysis of spatial genome organization. Histochem Cell Biol 123:229–238
Wiech T et al (2009) Spatial allelic imbalance of BCL2 genes and chromosome 18 territories in nonneoplastic and neoplastic cervical squamous epithelium. Eur Biophys J 38:793–806
Williams RR, Broad S, Sheer D, Ragoussis J (2002) Subchromosomal positioning of the epidermal differentiation complex (EDC) in keratinocyte and lymphoblast interphase nuclei. Exp Cell Res 272:163–175
Zeitz MJ, Ay F, Heidmann JD, Lerner PL, Noble WS, Steelman BN, Hoffman AR (2013) Genomic interaction profiles in breast cancer reveal altered chromatin architecture. PLoS One 8:e73974. doi:10.1371/journal.pone.0073974
Zink D et al (2004) Transcription-dependent spatial arrangement of CFTR and adjacent genes in human cell nuclei. J Cell Biol I166:815–825