Probing PML body function in ALT cells reveals spatiotemporal requirements for telomere recombination.
Open accessAbstract
Promyelocytic leukemia (PML) bodies (also called ND10) are dynamic nuclear structures implicated in a wide variety of cellular processes. ALT-associated PML bodies (APBs) are specialized PML bodies found exclusively in telomerase-negative tumors in which telomeres are maintained by recombination-based alternative (ALT) mechanisms. Although it has been suggested that APBs are directly implicated in telomere metabolism of ALT cells, their precise role and structure have remained elusive. Here we show that PML bodies in ALT cells associate with chromosome ends forming small, spatially well-defined clusters, containing on average 2–5 telomeres. Using an innovative approach that gently enlarges PML bodies in living cells while retaining their overall organization, we show that this physical enlargement of APBs spatially resolves the single telomeres in the cluster, but does not perturb the potential of the APB to recruit chromosome extremities. We show that telomere clustering in PML bodies is cell-cycle regulated and that unique telomeres within a cluster associate with recombination proteins. Enlargement of APBs induced the accumulation of telomere-telomere recombination intermediates visible on metaphase spreads and connecting heterologous chromosomes. The strand composition of these recombination intermediates indicated that this recombination is constrained to a narrow time window in the cell cycle following replication. These data provide strong evidence that PML bodies are not only a marker for ALT cells but play a direct role in telomere recombination, both by bringing together chromosome ends and by promoting telomere-telomere interactions between heterologous chromosomes.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
ALT-associated PML bodies have an essential role in telomere-lengthening in ALT+ cells by bringing chromosome ends together with recombination proteins.
“These ALT-associated PML bodies have an essential role in telomere-lengthening in ALT+ cells, by bringing chromosome ends together with the recombination proteins that mediate their lengthening (Draskovic et al., 2009; Osterwald et al., 2015).”
From USP7 Is a Master Regulator of Genome Stability (2020) · cites this paper as Draskovic et al., 2009
Cites
Cytokinesis-block micronucleus cytome assay
Fenech, M. F. (2007) · Nature Protocols · doi:10.1038/nprot.2007.77 · Cited by 2,025 · see citing works
Telomere maintenance by recombination in human cells
Dunham, M. A., Neumann, A. A., Fasching, C. L., & Reddel, R. R. (2000) · Nature Genetics · doi:10.1038/82586 · Cited by 879 · see citing works
Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies
Bernardi, R., & Pandolfi, P. P. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2277 · Cited by 876 · see citing works
Yeager, T. R., Neumann, A. A., Englezou, A., Huschtscha, L. I., Noble, J. R., & Reddel, R. R. (1999) · PubMed · Cited by 678 · see citing works
Alternative lengthening of telomeres in mammalian cells
Henson, J. D., Neumann, A. A., Yeager, T. R., & Reddel, R. R. (2002) · Oncogene · doi:10.1038/sj.onc.1205058 · Cited by 660 · see citing works
Purification of Proteins Associated with Specific Genomic Loci
Déjardin, J., & Kingston, R. E. (2009) · Cell · doi:10.1016/j.cell.2008.11.045 · Cited by 545 · see citing works
Funabiki, H., Hagan, I., Uzawa, S., & Yanagida, M. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.121.5.961 · Cited by 516 · see citing works
Homologous Recombination Generates T-Loop-Sized Deletions at Human Telomeres
Wang, R. C., Smogorzewska, A., & de Lange, T. (2004) · Cell · doi:10.1016/j.cell.2004.10.011 · Cited by 507 · see citing works
Everett, R. D., Freemont, P. S., Saitoh, H., Dasso, M., Orr, A., Kathoria, M., & Parkinson, J. (1998) · Journal of Virology · doi:10.1128/jvi.72.8.6581-6591.1998 · Cited by 399 · see citing works
Cooney, A. J., Tsai, S. Y., O’Malley, B. W., & Tsai, M. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.9.4153 · Cited by 383 · see citing works
Potts, P. R., & Yu, H. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1259 · Cited by 377 · see citing works
HSV‐1 IE protein Vmw110 causes redistribution of PML.
Everett, R. D., & Maul, G. G. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06835.x · Cited by 352 · see citing works
Buis, J. M., Wu, Y., Deng, Y., Leddon, J. L., Westfield, G., Eckersdorff, M., Sekiguchi, J., Chang, S. S., & Ferguson, D. O. (2008) · Cell · doi:10.1016/j.cell.2008.08.015 · Cited by 345 · see citing works
Telomeric DNA in ALT Cells Is Characterized by Free Telomeric Circles and Heterogeneous t-Loops
Cesare, A. J., & Griffith, J. D. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.22.9948-9957.2004 · Cited by 343 · see citing works
Alternative Lengthening of Telomeres Is Characterized by High Rates of Telomeric Exchange
Londoño‐Vallejo, A., Der‐Sarkissian, H., Cazes, L., Bacchetti, S., & Reddel, R. R. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-4035 · Cited by 319 · see citing works
Self-citationEverett, R. D., Earnshaw, W. C., Findlay, J., & Lomonte, P. (1999) · The EMBO Journal · doi:10.1093/emboj/18.6.1526 · Cited by 245 · see citing works
Self-citationLudérus, M. E. E., van Steensel, B., Chong, L., Sibon, O. C. M., Cremers, F. F. M., & de Lange, T. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.135.4.867 · Cited by 232 · see citing works
Visualizing telomere dynamics in living mammalian cells using PNA probes
Molenaar, C., Wiesmeijer, K. C., Verwoerd, N. P., Khazen, S., Eils, R., Tanke, H. J., & Dirks, R. W. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg633 · Cited by 217 · see citing works
Telomere maintenance by telomerase and by recombination can coexist in human cells
Cerone, M. A. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.18.1945 · Cited by 171 · see citing works
Grobelny, J. V., Godwin, A. K., & Broccoli, D. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.24.4577 · Cited by 161 · see citing works
Zhong, Z.-H., Jiang, W.-Q., Cesare, A. J., Neumann, A. A., Wadhwa, R., & Reddel, R. R. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701413200 · Cited by 159 · see citing works
Jiang, W.-Q., Zhong, Z.-H., Henson, J. D., Neumann, A. A., Chang, A. C.-M., & Reddel, R. R. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.7.2708-2721.2005 · Cited by 155 · see citing works
Luciani, J., Depetris, D., Usson, Y., Metzler‐Guillemain, C., Mignon‐Ravix, C., Mitchell, M. J., Mégarbané, A., Sardá, P., Sirma, H., Moncla, A., et al. (2006) · Journal of Cell Science · doi:10.1242/jcs.02965 · Cited by 132 · see citing works
Everett, R. D., Murray, J., Orr, A., & Preston, C. M. (2007) · Journal of Virology · doi:10.1128/jvi.00705-07 · Cited by 126 · see citing works
Jiang, W.-Q., Zh, Z., Henson, J. D., & Reddel, R. R. (2007) · Oncogene · doi:10.1038/sj.onc.1210260 · Cited by 115 · see citing works
Jegou, T., Chung, I., Heuvelman, G. L., Wachsmuth, M., Görisch, S. M., Greulich‐Bode, K. M., Boukamp, P., Lichter, P., & Rippe, K. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-02-0108 · Cited by 106 · see citing works
Dellaire, G. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg018 · Cited by 102 · see citing works
Fasching, C. L., Neumann, A. A., Muntoni, A., Yeager, T. R., & Reddel, R. R. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-1556 · Cited by 87 · see citing works
Cooney, A. J., Tsai, S. Y., O’Malley, B. W., & Tsai, M. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.9.4153-4163.1992 · Cited by 85 · see citing works
A human cell line that maintains telomeres in the absence of telomerase and of key markers of ALT
Cerone, M. A., Autexier, C., Londoño‐Vallejo, A., & Bacchetti, S. (2005) · Oncogene · doi:10.1038/sj.onc.1208934 · Cited by 71 · see citing works
Self-citationLive Cell Dynamics of Promyelocytic Leukemia Nuclear Bodies upon Entry into and Exit from Mitosis
Chen, Y.-C. M., Kappel, C., Beaudouin, J., Eils, R., & Spector, D. L. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-01-0035 · Cited by 54 · see citing works
PML nuclear bodies as sites of epigenetic regulation
Török, D. (2009) · Frontiers in bioscience · doi:10.2741/3311 · Cited by 51 · see citing works
Segmental Polymorphisms in the Proterminal Regions of a Subset of Human ChromosomesPreprint
Der‐Sarkissian, H., Vergnaud, G., Borde, Y.-M., Thomas, G. D., & Londoño‐Vallejo, A. (2002) · Genome Research · doi:10.1101/gr.322802 · Cited by 33 · see citing works
Self-citationAlternative ends: Telomeres and meiosis
Saint-André, C. D. L. R. (2007) · Biochimie · doi:10.1016/j.biochi.2007.08.010 · Cited by 22 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Alternative lengthening of telomeres: models, mechanisms and implications
Cesare, A. J., & Reddel, R. R. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2763 · Cited by 1,022 · see citing works
PML Nuclear BodiesPreprint
Lallemand-Breitenbach, V., & de Thé, H. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a000661 · Cited by 561 · see citing works
Interchromosomal Homology Searches Drive Directional ALT Telomere Movement and Synapsis
Cho, N. W., Dilley, R. L., Lampson, M. A., & Greenberg, R. A. (2014) · Cell · doi:10.1016/j.cell.2014.08.030 · Cited by 364 · see citing works
Telomeres and Telomere Length: A General Overview
Srinivas, N., Rachakonda, P. S., & Kumar, R. (2020) · Cancers · doi:10.3390/cancers12030558 · Cited by 313 · see citing works
Rapid induction of alternative lengthening of telomeres by depletion of the histone chaperone ASF1
O’Sullivan, R. J., Arnoult, N., Lackner, D. H., Oganesian, L., Haggblom, C., Corpet, A., Almouzni, G., & Karlseder, J. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2754 · Cited by 259 · see citing works
Self-citationTelomere length regulates TERRA levels through increased trimethylation of telomeric H3K9 and HP1α
Arnoult, N., Beneden, A. V., & Decottignies, A. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2364 · Cited by 258 · see citing works
Self-citationAlternative Lengthening of Telomeres through Two Distinct Break-Induced Replication Pathways
Zhang, J., Yadav, T., Ouyang, J., Lan, L., & Zou, L. (2019) · Cell Reports · doi:10.1016/j.celrep.2018.12.102 · Cited by 252 · see citing works
Barutcu, A. R., Lajoie, B. R., McCord, R. P., Tye, C. E., Hong, D., Messier, T. L., Browne, G., van Wijnen, A. J., Lian, J. B., Stein, J. L., et al. (2015) · Genome Biology · doi:10.1186/s13059-015-0768-0 · Cited by 250 · see citing works
ALTernative Telomere Maintenance and Cancer
Dilley, R. L., & Greenberg, R. A. (2015) · Trends in cancer · doi:10.1016/j.trecan.2015.07.007 · Cited by 241 · see citing works
Break-Induced Replication: The Where, The Why, and The How
Kramara, J., Osia, B., & Malkova, A. (2018) · Trends in Genetics · doi:10.1016/j.tig.2018.04.002 · Cited by 234 · see citing works
Assaying and investigating Alternative Lengthening of Telomeres activity in human cells and cancers
Henson, J. D., & Reddel, R. R. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.06.009 · Cited by 237 · see citing works
Acute promyelocytic leukemia, arsenic, and PML bodies
de Thé, H., Bras, M. L., & Lallemand-Breitenbach, V. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201112044 · Cited by 212 · see citing works
PML nuclear bodies and chromatin dynamics: catch me if you can!
Corpet, A., Kleijwegt, C., Roubille, S., Juillard, F., Jacquet, K., Texier, P., & Lomonte, P. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa828 · Cited by 204 · see citing works
Self-citationMolecular mechanisms of activity and derepression of alternative lengthening of telomeres
Pickett, H. A., & Reddel, R. R. (2015) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3106 · Cited by 203 · see citing works
Alternative lengthening of telomeres: from molecular mechanisms to therapeutic outlooks
Zhang, J., & Zou, L. (2020) · Cell & Bioscience · doi:10.1186/s13578-020-00391-6 · Cited by 181 · see citing works
Alternative Lengthening of Telomeres: DNA Repair Pathways Converge
Sobinoff, A. P., & Pickett, H. A. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.09.003 · Cited by 166 · see citing works
BLM and SLX4 play opposing roles in recombination‐dependent replication at human telomeres
Sobinoff, A. P., Allen, J. A. M., Neumann, A. A., Yang, S. F., Walsh, M. E., Henson, J. D., Reddel, R. R., & Pickett, H. A. (2017) · The EMBO Journal · doi:10.15252/embj.201796889 · Cited by 153 · see citing works
García-Expósito, L., Bournique, E., Bergoglio, V., Bose, A., González, J. B., Zhang, S., Roncaioli, J. L., Lee, M., Wallace, C. T., Watkins, S. C., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.10.048 · Cited by 141 · see citing works
NuRD–ZNF827 recruitment to telomeres creates a molecular scaffold for homologous recombination
Conomos, D., Reddel, R. R., & Pickett, H. A. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2877 · Cited by 129 · see citing works
SMARCAL1 Resolves Replication Stress at ALT Telomeres
Cox, K. E., Maréchal, A., & Flynn, R. L. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.011 · Cited by 123 · see citing works
Nuclear body phase separation drives telomere clustering in ALT cancer cells
Zhang, H., Zhao, R., Tones, J., Liu, M., Dilley, R. L., Chenoweth, D. M., Greenberg, R. A., & Lampson, M. A. (2020) · Molecular Biology of the Cell · doi:10.1091/mbc.e19-10-0589 · Cited by 119 · see citing works
USP7 Is a Master Regulator of Genome Stability
Valles, G. J., Bezsonova, I., Woodgate, R., & Ashton, N. W. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00717 · Cited by 114 · see citing works
Leung, J. W. C., Ghosal, G., Wang, W., Shen, X. H., Wang, J., Li, L., & Chen, J. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.411603 · Cited by 116 · see citing works
Protein phase separation and its role in tumorigenesis
Jiang, S., Fagman, J. B., Chen, C., Alberti, S., & Liu, B. (2020) · eLife · doi:10.7554/elife.60264 · Cited by 115 · see citing works
Nabetani, A., & Ishikawa, F. (2010) · The Journal of Biochemistry · doi:10.1093/jb/mvq119 · Cited by 113 · see citing works
Mutant IDH1 Promotes Glioma Formation In Vivo
Philip, B., Yu, D. X., Silvis, M. R., Shin, C., Robinson, J. P., Robinson, G. L., Welker, A., Angel, S. N., Tripp, S. R., Sonnen, J. A., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.133 · Cited by 112 · see citing works
Alternative lengthening of telomeres is a self-perpetuating process in ALT-associated PML bodies
Zhang, J., Genois, M., Ouyang, J., Lan, L., & Zou, L. (2021) · Molecular Cell · doi:10.1016/j.molcel.2020.12.030 · Cited by 111 · see citing works
USP7 - a crucial regulator of cancer hallmarks
Saha, G., Roy, S., Basu, M., & Ghosh, M. K. (2023) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2023.188903 · Cited by 106 · see citing works
Li, D., Nair, S. S., & Kumar, R. (2013) · Epigenetics · doi:10.4161/epi.24976 · Cited by 105 · see citing works
Chung, I., Osterwald, S., Deeg, K. I., & Rippe, K. (2012) · Nucleus · doi:10.4161/nucl.20326 · Cited by 100 · see citing works
Osterwald, S., Deeg, K. I., Chung, I., Parisotto, D., Wörz, S., Rohr, K., Erfle, H., & Rippe, K. (2015) · Journal of Cell Science · doi:10.1242/jcs.148296 · Cited by 92 · see citing works
SLX4IP Antagonizes Promiscuous BLM Activity during ALT Maintenance
Panier, S., Maric, M., Hewitt, G., Mason‐Osann, E., Gali, H., Dai, A., Labadorf, A. T., Guervilly, J.-H., Ruis, P., Segura‐Bayona, S., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.07.010 · Cited by 90 · see citing works
Alternative Lengthening of Telomeres: Building Bridges To Connect Chromosome Ends
Hoang, S. M., & O’Sullivan, R. J. (2020) · Trends in cancer · doi:10.1016/j.trecan.2019.12.009 · Cited by 83 · see citing works
ALT Positivity in Human Cancers: Prevalence and Clinical Insights
MacKenzie, D., Watters, A. K., To, J. T., Young, M. W., Muratori, J., Wilkoff, M. H., Abraham, R. G., Plummer, M. M., & Zhang, D. (2021) · Cancers · doi:10.3390/cancers13102384 · Cited by 85 · see citing works
Chung, I., Leonhardt, H., & Rippe, K. (2011) · Journal of Cell Science · doi:10.1242/jcs.084681 · Cited by 83 · see citing works
Wassing, I. E., & Esashi, F. (2020) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.08.010 · Cited by 79 · see citing works
Post-translational modifications of TRF1 and TRF2 and their roles in telomere maintenance
Walker, J. R., & Zhu, X. (2012) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2012.05.002 · Cited by 75 · see citing works
Compartmentalization of telomeres through DNA-scaffolded phase separation
Jack, A., Kim, Y., Strom, A. R., Lee, D. S. W., Williams, B. C., Schaub, J. M., Kellogg, E. H., Finkelstein, I. J., Ferro, L. S., Yıldız, A., et al. (2022) · Developmental Cell · doi:10.1016/j.devcel.2021.12.017 · Cited by 68 · see citing works
Repetitive RNAs as Regulators of Chromatin-Associated Subcompartment Formation by Phase Separation
Frank, L., & Rippe, K. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.04.015 · Cited by 68 · see citing works
Functions of BLM Helicase in Cells: Is It Acting Like a Double-Edged Sword?
Kaur, E., Agrawal, R., & Sengupta, S. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.634789 · Cited by 66 · see citing works
Temime‐Smaali, N., Guittat, L., Sidibe, A., Shin‐ya, K., Trentesaux, C., & Riou, J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006919 · Cited by 70 · see citing works
Assembly of telomeric chromatin to create ALTernative endings
O’Sullivan, R. J., & Almouzni, G. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.07.007 · Cited by 64 · see citing works
POT1-TPP1 telomere length regulation and disease
Aramburu, T. M., Plucinsky, S. M., & Skordalakes, E. (2020) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2020.06.040 · Cited by 56 · see citing works
Episkopou, H., Diman, A., Claude, E., Viceconte, N., & Decottignies, A. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.05.027 · Cited by 55 · see citing works
The role of post-translational modifications in fine-tuning BLM helicase function during DNA repair
Böhm, S., & Bernstein, K. A. (2014) · DNA repair · doi:10.1016/j.dnarep.2014.07.007 · Cited by 52 · see citing works
Mutations inhibiting KDM4B drive ALT activation in ATRX-mutated glioblastomas
Udugama, M., Hii, L. L., Garvie, A., Cervini, M., Vinod, B., Chan, F. L., Das, P. P., Mann, J. R., Collas, P., Voon, H. P. J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22543-z · Cited by 51 · see citing works
Telomeres and telomerase dance to the rhythm of the cell cycle
Londoño‐Vallejo, A., & Wellinger, R. J. (2012) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2012.05.004 · Cited by 50 · see citing works
Self-citationEmerging Implications of Phase Separation in Cancer
Ren, J., Zhang, Z., Zong, Z., Zhang, L., & Zhou, F. (2022) · Advanced Science · doi:10.1002/advs.202202855 · Cited by 47 · see citing works
Telomeres and viruses: common themes of genome maintenance
Deng, Z., Wang, Z., & Lieberman, P. M. (2012) · Frontiers in Oncology · doi:10.3389/fonc.2012.00201 · Cited by 45 · see citing works
Ferreira, H. C., Towbin, B. D., Jegou, T., & Gasser, S. M. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201307181 · Cited by 46 · see citing works
Mechanisms of Alternative Lengthening of TelomeresPreprint
O’Sullivan, R. J., & Greenberg, R. A. (2024) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041690 · Cited by 44 · see citing works
Lundberg, G., Sehic, D., Länsberg, J., Øra, I., Frigyesi, A., Castel, V., Navarro, S., Piqueras, M., Martinsson, T., Noguera, R., et al. (2011) · Genes Chromosomes and Cancer · doi:10.1002/gcc.20850 · Cited by 41 · see citing works
Segura‐Bayona, S., Villamor-Payà, M., Attolini, C. S., König, L. M., Sanchiz-Calvo, M., Boulton, S. J., & Stracker, T. H. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107983 · Cited by 39 · see citing works
Rapid and reversible suppression of ALT by DAXX in osteosarcoma cells
Yost, K. E., Soper, S. F. C., Walker, R. L., Pineda, M. A., Zhu, Y. J., Ester, C. D., Showman, S., Roschke, A. V., Waterfall, J. J., & Meltzer, P. S. (2019) · Scientific Reports · doi:10.1038/s41598-019-41058-8 · Cited by 40 · see citing works
Porreca, R. M., Herrera‐Moyano, E., Skourti, E., Law, P. P., Gonzalez-Franco, R., Montoya, A., Faull, P. A., Kramer, H., & Vannier, J. (2020) · eLife · doi:10.7554/elife.49817 · Cited by 37 · see citing works
Slatter, T. L., Gifford-Garner, J., Wiles, A. K., Tan, X., Chen, Y.-J., MacFarlane, M. R., Sullivan, M. J., Royds, J. A., & Hung, N. A. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.100468 · Cited by 36 · see citing works
Sun, L., Chiang, J. Y., Choi, J. Y., Xiong, Z., Mao, X., Collins, F. S., Hodes, R. J., & Cao, K. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907199116 · Cited by 37 · see citing works
New twists to the ALTernative endings at telomeres
Bhargava, R., Lynskey, M. L., & O’Sullivan, R. J. (2022) · DNA repair · doi:10.1016/j.dnarep.2022.103342 · Cited by 37 · see citing works
Telomere recombination and alternative telomere lengthening mechanisms
Londoño‐Vallejo, A. (2012) · Frontiers in bioscience · doi:10.2741/4084 · Cited by 36 · see citing works
Self-citationPML-mediated signaling and its role in cancer stem cells
Zhou, W., & Bao, S. (2013) · Oncogene · doi:10.1038/onc.2013.111 · Cited by 31 · see citing works
The human CTC1/STN1/TEN1 complex regulates telomere maintenance in ALT cancer cells
Huang, C., Jia, P., Chastain, M., Shiva, O., & Chai, W. (2017) · Experimental Cell Research · doi:10.1016/j.yexcr.2017.03.058 · Cited by 34 · see citing works
Chojak, R., Fares, J., Petrosyan, E., & Lesniak, M. S. (2023) · Journal of Neuro-Oncology · doi:10.1007/s11060-023-04387-3 · Cited by 30 · see citing works
Spatiotemporal multi-omics: exploring molecular landscapes in aging and regenerative medicine
Chu, L.-X., Wang, W.-J., Gu, X.-P., Wu, P., Gao, C., Zhang, Q., Wu, J., Jiang, D.-W., Huang, J.-Q., Ying, X.-W., et al. (2024) · Military Medical Research · doi:10.1186/s40779-024-00537-4 · Cited by 29 · see citing works
RPA shields inherited DNA lesions for post-mitotic DNA synthesis
Lezaja, A., Παναγόπουλος, Α., Wen, Y., Carvalho, E., Imhof, R., & Altmeyer, M. (2021) · Nature Communications · doi:10.1038/s41467-021-23806-5 · Cited by 27 · see citing works
González, J. B., García-Expósito, L., Galaviz, P., Lynskey, M. L., Allen, J. A. M., Hoang, S. M., Watkins, S. C., Pickett, H. A., & O’Sullivan, R. J. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.110088 · Cited by 27 · see citing works
Means to the ends: The role of telomeres and telomere processing machinery in metastasis
Robinson, N. J., & Schiemann, W. P. (2016) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2016.10.005 · Cited by 28 · see citing works
Telomeric recombination induced by dysfunctional telomeres
Brault, M. E., & Autexier, C. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e10-02-0173 · Cited by 27 · see citing works
Telomere Biology—Insights into an Intriguing Phenomenon
Venkatesan, S., Khaw, A. K., & Hande, M. P. (2017) · Cells · doi:10.3390/cells6020015 · Cited by 27 · see citing works
The dynamic and heterogeneous composition of biomolecular condensates and its functional relevance.
Sang, C. C., Upadhyay, S., Nosella, M. L., Forman-Kay, J., & Lee, H. O. (2025) · Nature reviews. Molecular cell biology · doi:10.1038/s41580-025-00897-2 · Cited by 34 · see citing works
The alternative lengthening of telomeres pathway may operate in non‐neoplastic human cells
Slatter, T. L., Tan, X., Yuen, Y. C., Gunningham, S. P., SiYan, S., Daly, E., Packer, S. G. K., Devenish, C. J., Royds, J. A., & Hung, N. A. (2011) · The Journal of Pathology · doi:10.1002/path.2981 · Cited by 26 · see citing works
The co-expression of telomerase and ALT pathway in human breast cancer tissues
Xu, B., Peng, M., & Song, Q. (2013) · Tumor Biology · doi:10.1007/s13277-013-1534-0 · Cited by 25 · see citing works
ALT: A Multi-Faceted Phenomenon
Sommer, A., & Royle, N. J. (2020) · Genes · doi:10.3390/genes11020133 · Cited by 25 · see citing works
XPF activates break-induced telomere synthesis
Guh, C.-Y., Shen, H.-J., Chen, L. W., Chiu, P.-C., Liao, I.-H., Lo, C.-C., Chen, Y., Hsieh, Y.-H., Chang, T.-C., Yen, C.-P., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33428-0 · Cited by 25 · see citing works
Li, F., Wang, Y., Hwang, I., Jang, J.-Y., Xu, L., Deng, Z., Yu, E. Y., Cai, Y., Wu, C., Han, Z., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37480-2 · Cited by 24 · see citing works
Nuclear Envelope and Chromatin, Lock and Key of Genome Integrity
Gay, S., & Foiani, M. (2015) · International review of cytology · doi:10.1016/bs.ircmb.2015.03.001 · Cited by 23 · see citing works
Synthetic lethality of cytolytic HSV-1 in cancer cells with ATRX and PML deficiency
Han, M., Napier, C. E., Frölich, S., Teber, E., Wong, T., Noble, J. R., Choi, E. H. Y., Everett, R. D., Cesare, A. J., & Reddel, R. R. (2019) · Journal of Cell Science · doi:10.1242/jcs.222349 · Cited by 23 · see citing works
Keeping up with the condensates: The retention, gain, and loss of nuclear membrane-less organelles
Lacroix, E., & Audas, T. E. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.998363 · Cited by 23 · see citing works
ATRX/DAXX: Guarding the Genome against the Hazards of ALT
Soper, S. F. C., & Meltzer, P. S. (2023) · Genes · doi:10.3390/genes14040790 · Cited by 23 · see citing works
Chromatin remodeling and spatial concerns in DNA double-strand break repair
Downs, J. A., & Gasser, S. M. (2024) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2024.102405 · Cited by 23 · see citing works
The role of SUMOylation in biomolecular condensate dynamics and protein localization
Gutierrez-Morton, E., & Wang, Y. (2024) · Cell Insight · doi:10.1016/j.cellin.2024.100199 · Cited by 22 · see citing works
Soranno, A., Incicco, J. J., Bona, P. D., Tomko, E. J., Galburt, E. A., Holehouse, A. S., & Galletto, R. (2021) · Journal of Molecular Biology · doi:10.1016/j.jmb.2022.167685 · Cited by 22 · see citing works
O’Hare, T. H., & Delany, M. E. (2011) · Cytogenetic and Genome Research · doi:10.1159/000330125 · Cited by 20 · see citing works
Vinagre, J., Nabais, J., Pinheiro, J., Batısta, R., Oliveira, R. C., Gonçalves, A. P., Pestana, A., Reis, M., Mesquita, B., Pinto, V. S., et al. (2016) · Scientific Reports · doi:10.1038/srep29714 · Cited by 19 · see citing works
Wilson, F. R., Ho, A., Walker, J. R., & Zhu, X. (2016) · Journal of Cell Science · doi:10.1242/jcs.186098 · Cited by 20 · see citing works
Dan, J., Zhou, Z.-C., Wang, F., Wang, H., Guo, R., Keefe, D., & Liu, L. (2022) · Cells · doi:10.3390/cells11030456 · Cited by 17 · see citing works
The Roles of Telomerase in the Generation of Polyploidy during Neoplastic Cell Growth
Christodoulidou, A., Raftopoulou, C., Chiourea, M., Papaioannou, G., Hoshiyama, H., Wright, W. E., Shay, J. W., & Gagos, S. (2013) · Neoplasia · doi:10.1593/neo.121398 · Cited by 19 · see citing works
TRIM28 inhibits alternative lengthening of telomere phenotypes by protecting SETDB1 from degradation
Wang, C., Songyang, Z., & Huang, Y. Y. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00660-y · Cited by 18 · see citing works
Telomeric function of mammalian telomerases at short telomeres
Fakhoury, J. J., Marie-Egyptienne, D. T., Londoño‐Vallejo, A., & Autexier, C. (2010) · Journal of Cell Science · doi:10.1242/jcs.063636 · Cited by 17 · see citing works
Self-citationZhao, R., Xu, M., Yu, X., Wondisford, A. R., Lackner, R. M., Salsman, J., Dellaire, G., Chenoweth, D. M., O’Sullivan, R. J., Zhao, X., et al. (2024) · Genes & Development · doi:10.1101/gad.351667.124 · Cited by 17 · see citing works
Osterwald, S., Wörz, S., Reymann, J., Sieckmann, F., Rohr, K., Erfle, H., & Rippe, K. (2011) · Biotechnology Journal · doi:10.1002/biot.201000474 · Cited by 16 · see citing works
Dynamics of telomeric chromatin at the crossroads of aging and cancer
Ye, J., Wu, Y., & Gilson, É. (2010) · Essays in Biochemistry · doi:10.1042/bse0480147 · Cited by 15 · see citing works
PITX1 Is a Regulator of TERT Expression in Prostate Cancer with Prognostic Power
Poos, A. M., Schroeder, C., Jaishankar, N., Röll, D., Oswald, M., Meiners, J., Braun, D. M., Knotz, C., Frank, L., Gunkel, M., et al. (2022) · Cancers · doi:10.3390/cancers14051267 · Cited by 16 · see citing works
Signalling inhibition by ponatinib disrupts productive alternative lengthening of telomeres (ALT)
Kusuma, F. K., Prabhu, A., Tieo, G., Ahmed, S. M., Dakle, P., Yong, W. K., Pathak, E., Madan, V., Jiang, Y. Y., Tam, W. L., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37633-3 · Cited by 15 · see citing works
Orphan nuclear receptors-induced ALT-associated PML bodies are targets for ALT inhibition
Gaela, V. M., Hsia, H.-Y., Joseph, N. A., Tzeng, W.-Y., Ting, P.-C., Shen, Y., Tsai, C.-T., Boudier, T., & Chen, L. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae389 · Cited by 15 · see citing works
ALT Telomeres Borrow from Meiosis to Get Moving
Arnoult, N., & Karlseder, J. (2014) · Cell · doi:10.1016/j.cell.2014.09.013 · Cited by 15 · see citing works
Self-citationBroderick, R., Cherdyntseva, V., Nieminuszczy, J., Dragona, E., Kyriakaki, M., Evmorfopoulou, T., Gagos, S., & Niedźwiedź, W. (2023) · Nature Communications · doi:10.1038/s41467-023-38029-z · Cited by 13 · see citing works
Kim, S., Park, S. H., Kang, N., Ra, J. S., Myung, K., & Lee, K. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae785 · Cited by 14 · see citing works
A new role for histone deacetylase 5 in the maintenance of long telomeres
Novo, C. L., Polese, C., Mathéus, N., Decottignies, A., Londoño‐Vallejo, A., Castronovo, V., & Mottet, D. (2013) · The FASEB Journal · doi:10.1096/fj.12-224204 · Cited by 14 · see citing works
Self-citationCHAMP1 complex directs heterochromatin assembly and promotes homology-directed DNA repair
Li, F., Zhang, T., Syed, A., Elbakry, A., Holmer, N., Nguyen, H., Mukkavalli, S., Greenberg, R. A., & D’Andrea, A. D. (2025) · Nature Communications · doi:10.1038/s41467-025-56834-6 · Cited by 13 · see citing works
Genome maintenance meets mechanobiology
Spegg, V., & Altmeyer, M. (2023) · Chromosoma · doi:10.1007/s00412-023-00807-5 · Cited by 13 · see citing works
- Authors
- Draskovic, I., Arnoult, N., Steiner, V., Bacchetti, S., Lomonte, P., & Londoño-Vallejo, A.
- Affiliations
- Institut Curie, 26 rue d'Ulm, 75248 Paris, France; Université Pierre et Marie Curie 06, 75005 Paris, France; Centre National de la Recherche Scientifique, Unité Mixte de Recherche 3244;
- Centre National de la Recherche Scientifique (FR)
- Instituto Nazionale Tumori Regina Elena (IT)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-09-15
- Volume
- 106
- Issue
- 37
- Pages
- 15726-15731
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2747187
- OpenAlex
- W2075977300
- Cited by
- 175
- References
- 34
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 15 · 2023: 15 · 2022: 11 · 2021: 18 · 2020: 13 · 2019: 12 · 2018: 2 · 2017: 7 · 2016: 10 · 2015: 8 · 2014: 8 · 2013: 10 · 2012: 13
- FWCI
- 7.07
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- PML bodies, ALT-associated PML bodies, telomere recombination, alternative lengthening of telomeres, telomere clustering, telomerase-negative cells, cell cycle regulation, recombination intermediates, ND10
- MeSH terms
- Promyelocytic Leukemia Protein, Cell Cycle, Cell Line, Humans, Nuclear Proteins, Recombination, Genetic, Transcription Factors, Telomere, In Situ Hybridization, Fluorescence, Fluorescent Antibody Technique, Indirect, Telomerase, Tumor Suppressor Proteins, Telomeric Repeat Binding Protein 2, Intranuclear Space, Cell Line, Tumor
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review