Quantification of telomere features in tumor tissue sections by an automated 3D imaging-based workflow

Palm, 2008, How shelterin protects mammalian telomeres, Annu. Rev. Genet., 42, 301, 10.1146/annurev.genet.41.110306.130350 Heidenreich, 2014, TERT promoter mutations in cancer development, Curr. Opin. Genet. Dev., 24, 30, 10.1016/j.gde.2013.11.005 Peifer, 2015, Telomerase activation by genomic rearrangements in high-risk neuroblastoma, Nature, 526, 700, 10.1038/nature14980 Valentijn, 2015, TERT rearrangements are frequent in neuroblastoma and identify aggressive tumors, Nat. Genet., 10.1038/ng.3438 Heaphy, 2011, Altered telomeres in tumors with ATRX and DAXX mutations, Science, 333, 425, 10.1126/science.1207313 Henson, 2010, Assaying and investigating alternative lengthening of telomeres activity in human cells and cancers, FEBS Lett., 584, 3800, 10.1016/j.febslet.2010.06.009 Dilley, 2015, Alternative telomere maintenance and cancer, Trends Cancer, 1, 145, 10.1016/j.trecan.2015.07.007 Bryan, 1995, Telomere elongation in immortal human cells without detectable telomerase activity, EMBO J., 14, 4240, 10.1002/j.1460-2075.1995.tb00098.x Chung, 2012, PML body meets telomere: the beginning of an ALTernate ending?, Nucleus, 3, 263, 10.4161/nucl.20326 Chung, 2011, De novo assembly of a PML nuclear subcompartment occurs through multiple pathways and induces telomere elongation, J. Cell Sci., 124, 3603, 10.1242/jcs.084681 Yeager, 1999, Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body, Cancer Res., 59, 4175 Lang, 2010, Three-dimensional organization of promyelocytic leukemia nuclear bodies, J. Cell Sci., 123, 392, 10.1242/jcs.053496 Lovejoy, 2012, Loss of ATRX, genome instability, and an altered DNA damage response are hallmarks of the alternative lengthening of telomeres pathway, PLoS Genet., 8, e1002772, 10.1371/journal.pgen.1002772 Sturm, 2012, Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma, Cancer Cell, 22, 425, 10.1016/j.ccr.2012.08.024 Schwartzentruber, 2012, Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma, Nature, 482, 226, 10.1038/nature10833 Cesare, 2004, Telomeric DNA in ALT cells is characterized by free telomeric circles and heterogeneous t-loops, Mol. Cell. Biol., 24, 9948, 10.1128/MCB.24.22.9948-9957.2004 Henson, 2009, DNA C-circles are specific and quantifiable markers of alternative-lengthening-of-telomeres activity, Nat. Biotechnol., 27, 1181, 10.1038/nbt.1587 Conomos, 2012, Variant repeats are interspersed throughout the telomeres and recruit nuclear receptors in ALT cells, J. Cell Biol., 199, 893, 10.1083/jcb.201207189 Pickett, 2015, Molecular mechanisms of activity and derepression of alternative lengthening of telomeres, Nat. Struct. Mol. Biol., 22, 875, 10.1038/nsmb.3106 Rippe, 2015, TERRA and the state of the telomere, Nat. Struct. Mol. Biol., 22, 853, 10.1038/nsmb.3078 Azzalin, 2007, Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends, Science, 318, 798, 10.1126/science.1147182 McDonald, 2010, Presence of alternative lengthening of telomeres mechanism in patients with glioblastoma identifies a less aggressive tumor type with longer survival, J. Neuropathol. Exp. Neurol., 69, 729, 10.1097/NEN.0b013e3181e576cf Dogeas, 2014, Alternative lengthening of telomeres predicts site of origin in neuroendocrine tumor liver metastases, J. Am. Coll. Surg., 218, 628, 10.1016/j.jamcollsurg.2014.01.001 Hakin-Smith, 2003, Alternative lengthening of telomeres and survival in patients with glioblastoma multiforme, Lancet, 361, 836, 10.1016/S0140-6736(03)12681-5 Sturm, 2014, Paediatric and adult glioblastoma: multiform (epi)genomic culprits emerge, Nat. Rev. Cancer, 14, 92, 10.1038/nrc3655 Meeker, 2002, Telomere length assessment in human archival tissues: combined telomere fluorescence in situ hybridization and immunostaining, Am. J. Pathol., 160, 1259, 10.1016/S0002-9440(10)62553-9 Heaphy, 2011, The potential utility of telomere-related markers for cancer diagnosis, J. Cell Mol. Med., 15, 1227, 10.1111/j.1582-4934.2011.01284.x Cesare, 2015, Visualization of telomere integrity and function in vitro and in vivo using immunofluorescence techniques, Curr. Protoc. Cytom., 73 Heaphy, 2011, Prevalence of the alternative lengthening of telomeres telomere maintenance mechanism in human cancer subtypes, Am. J. Pathol., 179, 1608, 10.1016/j.ajpath.2011.06.018 Pezzolo, 2015, Intratumoral diversity of telomere length in individual neuroblastoma tumors, Oncotarget, 6, 7493, 10.18632/oncotarget.2115 Zhou, 2012, Telomere length variation in normal epithelial cells adjacent to tumor: potential biomarker for breast cancer local recurrence, Carcinogenesis, 33, 113, 10.1093/carcin/bgr248 Heaphy, 2013, Prostate cancer cell telomere length variability and stromal cell telomere length as prognostic markers for metastasis and death, Cancer Discov., 3, 1130, 10.1158/2159-8290.CD-13-0135 Joshua, 2007, Telomere attrition in isolated high-grade prostatic intraepithelial neoplasia and surrounding stroma is predictive of prostate cancer, Neoplasia, 9, 81, 10.1593/neo.06745 Osterwald, 2015, PML induces compaction, TRF2 depletion and DNA damage signaling at telomeres and promotes their alternative lengthening, J. Cell Sci., 128, 1887, 10.1242/jcs.148296 Osterwald, 2012, A three-dimensional colocalization RNA interference screening platform to elucidate the alternative lengthening of telomeres pathway, Biotechnol. J., 7, 103, 10.1002/biot.201000474 Kononen, 1998, Tissue microarrays for high-throughput molecular profiling of tumor specimens, Nat. Med., 4, 844, 10.1038/nm0798-844 Ovesny, 2014, ThunderSTORM: a comprehensive ImageJ plug-in for PALM and STORM data analysis and super-resolution imaging, Bioinformatics, 30, 2389, 10.1093/bioinformatics/btu202 Wörz, 2010, 3D Geometry-based quantification of colocalizations in multi-channel 3D microscopy images of human soft tissue tumors, IEEE Trans. Medical Imaging, 29, 1474, 10.1109/TMI.2010.2049857 Eck, 2016, A spherical harmonics intensity model for 3D segmentation and 3D shape analysis of heterochromatin foci, Med. Image Anal., 32, 18, 10.1016/j.media.2016.03.001 Cerone, 2005, A human cell line that maintains telomeres in the absence of telomerase and of key markers of ALT, Oncogene, 24, 7893, 10.1038/sj.onc.1208934 Fasching, 2005, Telomerase-independent telomere length maintenance in the absence of alternative lengthening of telomeres-associated promyelocytic leukemia bodies, Cancer Res., 65, 2722, 10.1158/0008-5472.CAN-04-2881 Marciniak, 2005, A novel telomere structure in a human alternative lengthening of telomeres cell line, Cancer Res., 65, 2730, 10.1158/0008-5472.CAN-04-2888 Viegas, 2007, An improved and cost-effective methodology for the reduction of autofluorescence in direct immunofluorescence studies on formalin-fixed paraffin-embedded tissues, Eur. J. Histochem., 51, 59 Abedalthagafi, 2013, The alternative lengthening of telomere phenotype is significantly associated with loss of ATRX expression in high-grade pediatric and adult astrocytomas: a multi-institutional study of 214 astrocytomas, Mod. Pathol., 26, 1425, 10.1038/modpathol.2013.90 Betzig, 2006, Imaging intracellular fluorescent proteins at nanometer resolution, Science, 313, 1642, 10.1126/science.1127344 Lemmer, 2008, SPDM: light microscopy with single-molecule resolution at the nanoscale, Appl. Phys. B, 93, 1, 10.1007/s00340-008-3152-x Heilemann, 2008, Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes, Angew. Chem. Int. Ed. Engl., 47, 6172, 10.1002/anie.200802376 Folling, 2008, Fluorescence nanoscopy by ground-state depletion and single-molecule return, Nat. Methods, 5, 943, 10.1038/nmeth.1257 Rust, 2006, Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM), Nat. Methods, 3, 793, 10.1038/nmeth929 Lallemand-Breitenbach, 2010, PML nuclear bodies, Cold Spring Harb. Perspect. Biol., 2, a000661, 10.1101/cshperspect.a000661 Dempsey, 2011, Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging, Nat. Methods, 8, 1027, 10.1038/nmeth.1768 Gunkel, 2009, Dual color localization microscopy of cellular nanostructures, Biotechnol. J., 4, 927, 10.1002/biot.200900005 Malkusch, 2012, Coordinate-based colocalization analysis of single-molecule localization microscopy data, Histochem. Cell Biol., 137, 1, 10.1007/s00418-011-0880-5 Flottmann, 2013, Correlative light microscopy for high-content screening, Biotechniques, 55, 243, 10.2144/000114099 Meeker, 2002, Telomere shortening is an early somatic DNA alteration in human prostate tumorigenesis, Cancer Res., 62, 6405 Fordyce, 2005, Association between cancer-free survival and telomere DNA content in prostate tumors, J. Urol., 173, 610, 10.1097/01.ju.0000143195.49685.ce Heaphy, 2015, Prostate stromal cell telomere shortening is associated with risk of prostate cancer in the placebo arm of the Prostate Cancer Prevention Trial, Prostate, 75, 1160, 10.1002/pros.22997