Alternative lengthening of telomeres (ALT) influences survival in soft tissue sarcomas: a systematic review with meta-analysis
Open accessAbstract
BACKGROUND: Alternative lengthening of telomeres (ALT) is a telomerase-independent mechanism used by a broad range of neoplasms to maintain telomere length, permitting uncontrolled replication during their progression. ALT has been described in different types of sarcoma, but a comprehensive analysis of its clinical significance is still lacking. Therefore, we provide here the first meta-analysis on this topic. METHODS: We searched SCOPUS and PubMed through July 2018 to identify all studies that investigated the prognostic role of ALT in sarcomas. We considered the risk of death (risk ratio, RR) calculated as the number of death vs. total participants during follow-up in ALT+ versus ALT- patients as the primary outcome. The secondary outcome was the hazard ratio (HR), adjusted for the maximum number of covariates available, using ALT- patients as reference. RESULTS: Eight articles comprising a total of 551 patients with sarcomas (226 ALT+ and 325 ALT-) were selected. The ALT+ group showed a higher mitotic count and a higher tumor grade compared with the ALT- group (p < 0.01). Furthermore, we demonstrate a strong impact of ALT on survival. In fact, ALT+ patients showed a statistically significant higher risk of death than ALT- patients, when also considering data from multivariate analyses (RR = 1.50; 95% CI: 1.15-1.96; p = 0.003; HR = 2.02; 95% CI: 1.22-3.38; p = 0.007). CONCLUSIONS: Our results indicate that ALT is associated with an increased risk of death in patients with sarcoma. In these neoplasms, ALT should be taken into account for a precise prognostic stratification and design of potential therapeutic strategies.
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Deletion of ATRX seems to activate alternative lengthening of telomeres and is associated with decreased survival in osteosarcoma.
“deletion of ATRX, which seems to activate alternative lengthening of telomeres and is associated with decreased survival 36,43 .”
From Osteosarcoma (2022) · cites this paper as [43]
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Bias in meta-analysis detected by a simple, graphical test
Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997) · BMJ · doi:10.1136/bmj.315.7109.629 · Cited by 56,722 · see citing works
Meta-analysis in clinical trials
DerSimonian, R., & Laird, N. (1986) · Controlled Clinical Trials · doi:10.1016/0197-2456(86)90046-2 · Cited by 39,552 · see citing works
Quantifying heterogeneity in a meta‐analysis
Higgins, J. P. T., & Thompson, S. G. (2002) · Statistics in Medicine · doi:10.1002/sim.1186 · Cited by 36,763 · see citing works
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P. C., Ioannidis, J. P. A., Clarke, M., Devereaux, P. J., Kleijnen, J., & Moher, D. (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000100 · Cited by 28,164 · see citing works
Dermyshi, E., Wang, Y., Yan, C., Hong, W., Qiu, G., Gong, X., & Zhang, T. (2017) · Neonatology · doi:10.1159/000454668 · Cited by 24,577 · see citing works
Stroup, D. F. (2000) · JAMA · doi:10.1001/jama.283.15.2008 · Cited by 20,623 · see citing works
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gotzsche, P. C., Ioannidis, J. P. A., Clarke, M., Devereaux, P. J., Kleijnen, J., & Moher, D. (2009) · BMJ · doi:10.1136/bmj.b2700 · Cited by 17,648 · see citing works
Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma
Schwartzentruber, J., Korshunov, A., Liu, X.-Y., Jones, D. T. W., Pfaff, E., Jacob, K., Sturm, D., Fontebasso, A. M., Quang, D.-A. K., Tönjes, M., et al. (2012) · Nature · doi:10.1038/nature10833 · Cited by 2,631 · see citing works
ATM, ATR, and DNA-PK: The Trinity at the Heart of the DNA Damage Response
Blackford, A. N., & Jackson, S. P. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.05.015 · Cited by 1,953 · see citing works
A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis
Greider, C. W., & Blackburn, E. H. (1989) · Nature · doi:10.1038/337331a0 · Cited by 1,643 · see citing works
Rindi, G., Klimstra, D. S., Abedi‐Ardekani, B., Asa, S. L., Bosman, F. T., Brambilla, E. M., BUSAM, K. J., de Krijger, R. R., Dietel, M., El‐Naggar, A. K., et al. (2018) · Modern Pathology · doi:10.1038/s41379-018-0110-y · Cited by 1,164 · see citing works
Altered Telomeres in Tumors with <i>ATRX</i> and <i>DAXX</i> Mutations
Heaphy, C. M., de Wilde, R. F., Jiao, Y., Klein, A. P., Edil, B. H., Shi, C., Bettegowda, C., Rodriguez, F. J., Eberhart, C. G., Hebbar, S., et al. (2011) · Science · doi:10.1126/science.1207313 · Cited by 1,083 · see citing works
Whole-genome landscape of pancreatic neuroendocrine tumours
Initiative, A. P. C. G., Scarpa, A., Chang, D. K., Nones, K., Corbo, V., Patch, A.-M., Bailey, P., Lawlor, R. T., Johns, A. L., Miller, D. K., et al. (2017) · Nature · doi:10.1038/nature21063 · Cited by 999 · see citing works
Self-citationLuchini, C., Stubbs, B., Solmi, M., & Veronese, N. (2017) · World Journal of Meta-Analysis · doi:10.13105/wjma.v5.i4.80 · Cited by 977 · see citing works
Self-citationYeager, 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
Selective killing of ATM- or p53-deficient cancer cells through inhibition of ATR
Reaper, P. M., Griffiths, M. R., Long, J. M., Charrier, J.-D., MacCormick, S., Charlton, P. A., Golec, J. M. C., & Pollard, J. R. (2011) · Nature Chemical Biology · doi:10.1038/nchembio.573 · Cited by 633 · see citing works
Telomere Shortening Is Associated with Cell Division in Vitro and in Vivo
Allsopp, R. C., Chang, E., Kashefi-Aazam, M., Rogaev, E. I., Piatyszek, M. A., Shay, J. W., & Harley, C. B. (1995) · Experimental Cell Research · doi:10.1006/excr.1995.1306 · Cited by 533 · see citing works
Shay, J. W. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.7.677 · Cited by 517 · see citing works
Heaphy, C. M., Subhawong, A. P., Hong, S.-M., Goggins, M. G., Montgomery, E. A., Gabrielson, E., Netto, G. J., Epstein, J. I., Lotan, T. L., Westra, W. H., et al. (2011) · The American Journal of Pathology · doi:10.1016/j.ajpath.2011.06.018 · Cited by 516 · see citing works
Alternative lengthening of telomeres renders cancer cells hypersensitive to ATR inhibitors
Flynn, R. L., Cox, K. E., Jeitany, M., Wakimoto, H., Bryll, A. R., Ganem, N. J., Bersani, F., Pineda, J. R., Suvà, M. L., Benes, C. H., et al. (2015) · Science · doi:10.1126/science.1257216 · Cited by 504 · see citing works
Evidence for a Critical Telomere Length in Senescent Human Fibroblasts
Allsopp, R., & Harley, C. B. (1995) · Experimental Cell Research · doi:10.1006/excr.1995.1213 · Cited by 391 · see citing works
Fokas, E., Prevo, R., Pollard, J. R., Reaper, P. M., Charlton, P., Cornelissen, B. T., Vallis, K. A., Hammond, E. M., Olcina, M. M., McKenna, W. G., et al. (2012) · Cell Death and Disease · doi:10.1038/cddis.2012.181 · Cited by 372 · see citing works
Lecona, E., & Fernández-Capetillo, Ó. (2018) · Nature reviews. Cancer · doi:10.1038/s41568-018-0034-3 · Cited by 327 · see citing works
Henson, J. D., Hannay, J. A. F., McCarthy, S. W., Royds, J. A., Yeager, T. R., Robinson, R. A., Wharton, S. B., Jellinek, D. A., Arbuckle, S. M., Yoo, J., et al. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.217.11.1 · Cited by 304 · see citing works
Charrier, J., Durrant, S. J., Golec, J. M. C., Kay, D. P., Knegtel, R. M. A., MacCormick, S., Mortimore, M., O'Donnell, M. E., Pinder, J. L., Reaper, P. M., et al. (2011) · Journal of Medicinal Chemistry · doi:10.1021/jm101488z · Cited by 256 · see citing works
Singhi, A. D., Liu, T., Roncaioli, J. L., Cao, D., Zeh, H. J., Zureikat, A. H., Tsung, A., Marsh, J. W., Lee, K. K. W., Hogg, M. E., et al. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-1113 · Cited by 250 · see citing works
Genetics and Epigenetics of Gastroenteropancreatic Neuroendocrine Neoplasms
Mafficini, A., & Scarpa, A. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00160 · Cited by 215 · see citing works
Molecular 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
Telomerase in cancer and aging
Granger, M. P., Wright, W. E., & Shay, J. W. (2002) · Critical Reviews in Oncology/Hematology · doi:10.1016/s1040-8428(01)00188-3 · Cited by 159 · see citing works
Kim, J. Y., Brosnan‐Cashman, J. A., An, S., Kim, S. J., Song, K. B., Kim, M. S., Kim, M.-J., Hwang, D. W., Meeker, A. K., Yu, E., et al. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-1147 · Cited by 151 · see citing works
Costa, A., Daidone, M. G., Daprai, L., Villa, R., Cantù, S., Pilotti, S., Mariani, L., Gronchi, A., Henson, J. D., Reddel, R. R., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0273 · Cited by 138 · see citing works
Exome Sequencing of Uterine Leiomyosarcomas Identifies Frequent Mutations in TP53, ATRX, and MED12
Mäkinen, N., Aavikko, M., Heikkinen, T., Taipale, M., Taipale, J., Koivisto-Korander, R., Bützow, R. C., & Vahteristo, P. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005850 · Cited by 138 · see citing works
Telomere Maintenance Mechanisms in Cancer
Gaspar, T. B., Sá, A., Lopes, J. M., Sobrinho-Simões, M. A., Soares, P., & Vinagre, J. (2018) · Genes · doi:10.3390/genes9050241 · Cited by 132 · see citing works
WHO Classification of Soft Tissue and Bone, fourth edition
Rosenberg, A. E. (2013) · Current Opinion in Oncology · doi:10.1097/01.cco.0000432522.16734.2d · Cited by 119 · see citing works
Telomerase Expression Predicts Unfavorable Outcome in Osteosarcoma
Sanders, R. P., Drissi, R., Billups, C. A., Daw, N. C., Valentine, M. B., & Dome, J. S. (2004) · Journal of Clinical Oncology · doi:10.1200/jco.2004.03.043 · Cited by 108 · see citing works
Liau, J., Tsai, J., Jeng, Y., Lee, J., Hsu, H.-H., & Yang, C. (2014) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000000324 · Cited by 101 · see citing works
Pea, A., Yu, J., Marchionni, L., Noë, M., Luchini, C., Pulvirenti, A., de Wilde, R. F., Brosens, L. A. A., Rezaee, N., Javed, A. A., et al. (2018) · Annals of Surgery · doi:10.1097/sla.0000000000003022 · Cited by 97 · see citing works
Self-citationLiau, J., Lee, J., Tsai, J., Yang, C., Liu, T., Ke, Z.-L., Hsu, H.-H., & Jeng, Y. (2015) · Modern Pathology · doi:10.1038/modpathol.2015.114 · Cited by 87 · 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
Lee, J., Jeng, Y., Liau, J., Tsai, J., Hsu, H.-H., & Yang, C. (2015) · Modern Pathology · doi:10.1038/modpathol.2015.67 · Cited by 58 · see citing works
Liau, J., Tsai, J., Yang, C., Lee, J., Liang, C., Hsu, H.-H., & Jeng, Y. (2015) · Human Pathology · doi:10.1016/j.humpath.2015.05.019 · Cited by 53 · see citing works
Mangerel, J., Price, A. J., Castelo‐Branco, P., Brzezinski, J. J., Buczkowicz, P., Rakopoulos, P., Merino, D. M., Baskin, B., Wasserman, J. D., Mistry, M., et al. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1348-1 · Cited by 52 · see citing works
Next-Generation Histopathologic Diagnosis: A Lesson From a Hepatic Carcinosarcoma
Luchini, C., Capelli, P., Fassan, M., Simbolo, M., Mafficini, A., Pedica, F., Ruzzenente, A., Guglielmi, A., Corbo, V., & Scarpa, A. (2014) · Journal of Clinical Oncology · doi:10.1200/jco.2012.47.5855 · Cited by 50 · see citing works
Self-citationSlatter, T. L., Hsia, H., Samaranayaka, A., Sykes, P. H., Clow, W. M., Devenish, C. J., Sutton, T., Royds, J. A., Ip, P. P. C., Cheung, A., et al. (2015) · The Journal of Pathology Clinical Research · doi:10.1002/cjp2.11 · Cited by 48 · see citing works
Targeting Telomerase and ATRX/DAXX Inducing Tumor Senescence and Apoptosis in the Malignant Glioma
Fan, H., Chen, C., Chi, C.-S., Tsai, J., Chiang, K.-L., Chang, Y., Lin, S., & Harn, H. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20010200 · Cited by 45 · see citing works
Exploring heterogeneity in meta‐analyses: needs, resources and challenges
Xu, H., Platt, R. W., Luo, Z., Wei, S. Q., & Fraser, W. D. (2008) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2007.00908.x · Cited by 38 · see citing works
Alternative lengthening of telomeres phenotype and loss of ATRX expression in sarcomas (Review)
Ren, X., Tu, C., Tang, Z., Ma, R., & Li, Z. (2018) · Oncology Letters · doi:10.3892/ol.2018.8318 · Cited by 30 · see citing works
Telomere-Maintenance Mechanisms in Soft-Tissue Malignant Fibrous Histiocytomas
Matsuo, T., Shay, J. W., Wright, W. E., Hiyama, E., Shimose, S., Kubo, T., Sugita, T., Yasunaga, Y., & Ochi, M. (2009) · Journal of Bone and Joint Surgery · doi:10.2106/jbjs.g.01390 · Cited by 29 · see citing works
Lee, Y., Park, N.-H., & Lee, H. (2012) · International Journal of Gynecological Cancer · doi:10.1097/igc.0b013e31823ca017 · Cited by 29 · see citing works
Venturini, L., Daidone, M. G., Motta, R., Cimino-Reale, G., Hoare, S. F., Gronchi, A., Folini, M., Keith, W. N., & Zaffaroni, N. (2012) · Neuro-Oncology · doi:10.1093/neuonc/nos083 · Cited by 28 · see citing works
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Beird, H. C., Bielack, S. S., Flanagan, A. M., Gill, J., Heymann, D., Janeway, K. A., Livingston, J. A., Roberts, R. D., Strauss, S. J., & Gorlick, R. (2022) · Nature Reviews Disease Primers · doi:10.1038/s41572-022-00409-y · Cited by 660 · see citing works
Targeting telomeres: advances in telomere maintenance mechanism-specific cancer therapies
Gao, J., & Pickett, H. A. (2022) · Nature reviews. Cancer · doi:10.1038/s41568-022-00490-1 · Cited by 209 · see citing works
Aguilera, P., & Lopez-Contreras, A. J. (2023) · Trends in Genetics · doi:10.1016/j.tig.2023.02.009 · Cited by 111 · see citing works
Feasibility of whole genome and transcriptome profiling in pediatric and young adult cancers
Shukla, N. N., Levine, M. F., Gundem, G., Domenico, D., Spitzer, B. G., Bouvier, N., Ossa, J. A., Głodzik, D., Medina-Martinez, J. S., Bhanot, U. K., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30233-7 · Cited by 70 · see citing works
Telomere maintenance mechanisms in cancer: telomerase, ALT or lack thereof
Claude, E., & Decottignies, A. (2020) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.01.002 · Cited by 60 · see citing works
Koneru, B., Farooqi, A. S., Nguyen, T. H., Chen, W. H., Hindle, A., Eslinger, C. R., Makena, M. R., Burrow, T. A., Wilson, J., Smith, A., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abd5750 · Cited by 58 · see citing works
G-quadruplexes mark alternative lengthening of telomeres
Yang, S. Y. C., Chang, E. Y., Lim, J., Kwan, H., Monchaud, D., Yip, S. S. F., Stirling, P. C., & Wong, J. M. Y. (2021) · NAR Cancer · doi:10.1093/narcan/zcab031 · Cited by 57 · see citing works
Alternative Lengthening of Telomeres (ALT) in Tumors and Pluripotent Stem Cells
Zhao, S., Wang, F., & Liu, L. (2019) · Genes · doi:10.3390/genes10121030 · Cited by 41 · see citing works
Recagni, M., Bidzińska, J., Zaffaroni, N., & Folini, M. (2020) · Cancers · doi:10.3390/cancers12040949 · Cited by 41 · see citing works
Alternative lengthening of telomeres: mechanism and the pathogenesis of cancer
Mori, J., Keegan, J., Flynn, R. L., & Heaphy, C. M. (2023) · Journal of Clinical Pathology · doi:10.1136/jcp-2023-209005 · Cited by 34 · see citing works
Ali, J. H., & Walter, M. (2023) · Cancer Cell International · doi:10.1186/s12935-023-03041-2 · Cited by 32 · see citing works
Bioinformatics workflows for clinical applications in precision oncology
Jäger, N. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2020.12.020 · Cited by 31 · see citing works
ALT control, delete: FANCM as an anti-cancer target in Alternative Lengthening of Telomeres
O’Rourke, J. J., Bythell‐Douglas, R., Dunn, E. A., & Deans, A. J. (2019) · Nucleus · doi:10.1080/19491034.2019.1685246 · Cited by 31 · see citing works
hTERT promoter methylation promotes small cell lung cancer progression and radiotherapy resistance
Zhai, G., Li, J., Zheng, J., An, P., Chen, X., Wang, X., & Li, C. (2020) · Journal of Radiation Research · doi:10.1093/jrr/rraa052 · Cited by 29 · see citing works
Luchini, C., Lawlor, R. T., Bersani, S., Vicentini, C., Paolino, G., Mattiolo, P., Pea, A., Cingarlini, S., Milella, M., & Scarpa, A. (2021) · Current Oncology Reports · doi:10.1007/s11912-021-01096-w · Cited by 29 · see citing works
Self-citationHolesova, Z., Krasničanová, L., Saade, R., Pös, O., Budiš, J., Gazdarica, J., Repiská, V., & Szemes, T. (2023) · Genes · doi:10.3390/genes14030715 · Cited by 28 · see citing works
Pan-Cancer Analysis of Alternative Lengthening of Telomere Activity
Sung, J., Lim, H., Joung, J., & Park, W. (2020) · Cancers · doi:10.3390/cancers12082207 · Cited by 26 · see citing works
Telomere dynamics in the first year of life, but not later in life, predict lifespan in a wild bird
Sheldon, E. L., Eastwood, J. R., Teunissen, N., Roast, M. J., Aranzamendi, N. H., Fan, M., Hall, M. L., Kingma, S. A., Verhulst, S., & Peters, A. (2021) · Molecular Ecology · doi:10.1111/mec.16296 · Cited by 26 · 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
Shelterin complex gene: Prognosis and therapeutic vulnerability in cancer
Bhari, V. K., Kumar, D., Kumar, S., & Mishra, R. (2021) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2021.100937 · Cited by 24 · see citing works
FANCM branchpoint translocase: Master of traverse, reverse and adverse DNA repair
Abbouche, L., Bythell‐Douglas, R., & Deans, A. J. (2024) · DNA repair · doi:10.1016/j.dnarep.2024.103701 · Cited by 20 · see citing works
The Future of Targeted Therapy for Leiomyosarcoma
Denu, R. A., Dann, A. M., Keung, E. Z.-Y., Nakazawa, M. S., & Nassif, E. F. (2024) · Cancers · doi:10.3390/cancers16050938 · Cited by 19 · see citing works
Aschacher, T., Wolf, B., Aschacher, O., Enzmann, F., László, V., Meßner, B., Türkcan, A., Weis, S., Spiegl‐Kreinecker, S., Holzmann, K., et al. (2019) · Neoplasia · doi:10.1016/j.neo.2019.11.002 · Cited by 17 · see citing works
The hallmarks of oncogenic signaling: From pathways to resistance in cancer therapy
Tufail, M., Gong, K., Ijaz, B., Patel, H. H., Lui, W., Wang, X., & Li, J. (2026) · Drug Resistance Updates · doi:10.1016/j.drup.2026.101355 · Cited by 16 · see citing works
Matsuda, Y., Ye, J., Yamakawa, K., Mukai, Y., Azuma, K., Wu, L., Masutomi, K., Yamashita, T., Daigo, Y., Miyagi, Y., et al. (2022) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djac226 · Cited by 15 · see citing works
TCGA Pan-Cancer Genomic Analysis of Alternative Lengthening of Telomeres (ALT) Related Genes
Armendáriz‐Castillo, I., López‐Cortés, A., García-Cárdenas, J. M., Guevara‐Ramírez, P., Leone, P., Pérez‐Villa, A., Yumiceba, V., Zambrano, A. K., Guerrero, S. X., & Paz‐y‐Miño, C. (2020) · Genes · doi:10.3390/genes11070834 · Cited by 14 · see citing works
Unravelling undifferentiated soft tissue sarcomas: insights from genomics
Hames-Fathi, S., Nottley, S. W. G., & Pillay, N. (2021) · Histopathology · doi:10.1111/his.14446 · Cited by 12 · see citing works
Burrow, T. A., Koneru, B., Macha, S. J., Sun, W., Barr, F. G., Triche, T. J., & Reynolds, C. P. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1399442 · Cited by 9 · see citing works
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Sung, J. (2025) · Cells · doi:10.3390/cells14201613 · Cited by 8 · see citing works
Crende, O., García-Gallastegui, P., Luzuriaga, J., Badiola, I., de la Hoz, C., Unda, F., Ibarretxe, G., & Pineda, J. R. (2020) · Biology · doi:10.3390/biology9120426 · Cited by 8 · see citing works
Bicanová, L., Kreilmeier‐Berger, T., Reifinger, M., Holzmann, K., & KLEITER, M. M. (2020) · Veterinary and Comparative Oncology · doi:10.1111/vco.12665 · Cited by 7 · see citing works
Heaphy, C. M., Patel, S., Smith, K., Wondisford, A. R., Lynskey, M. L., O’Sullivan, R. J., Fuhrer, K., Han, X., Seethala, R. R., Liu, T., et al. (2024) · Modern Pathology · doi:10.1016/j.modpat.2024.100651 · Cited by 6 · see citing works
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Pierpoint, M., Floyd, W., Wisdom, A. J., Luo, L., Ma, Y., Dickson, B. C., Waitkus, M. S., & Kirsch, D. G. (2025) · iScience · doi:10.1016/j.isci.2025.112357 · Cited by 5 · see citing works
Alternative lengthening of telomeres confers favorable prognosis in chondrosarcomas
Sung, J., Kim, J., & Kim, Y. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-06539-7 · Cited by 5 · see citing works
Zeng, F., Chen, Y., & Lin, J. (2024) · BMC Cancer · doi:10.1186/s12885-024-13146-0 · Cited by 4 · see citing works
Using Transcriptional Signatures to Find Cancer Drivers with LURE
Haan, D., Tao, R., Friedl, V., Anastopoulos, I. N., Wong, C. K., Weinstein, A. S., & Stuart, J. M. (2019) · Pacific Symposium on Biocomputing (PSB) · doi:10.1142/9789811215636_0031 · Cited by 4 · see citing works
A Role for Human DNA Polymerase λ in Alternative Lengthening of Telomeres
Mentegari, E., Bertoletti, F., Kiššová, M., Zucca, E., Galli, S., Tagliavini, G., Garbelli, A., Maffia, A., Bione, S., Ferrari, E. S., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052365 · Cited by 4 · see citing works
Telomere maintenance mechanism subtype reveals different immune activity in vestibular schwannoma
Sung, J., & Lee, J. W. (2023) · Journal of Neuro-Oncology · doi:10.1007/s11060-023-04458-5 · Cited by 3 · see citing works
Guo, Y.-Z., Zhang, Y., Wang, Q., Yu, J., Wan, Q., Huang, J., & Fang, S. (2022) · iScience · doi:10.1016/j.isci.2022.105850 · Cited by 3 · see citing works
Mattis, N., Goncalves, T., Kim, K., Hammond, E. M., & Rose, A. M. (2025) · Human Molecular Genetics · doi:10.1093/hmg/ddaf118 · Cited by 2 · see citing works
Telomere Dynamics in Post-Traumatic Stress Disorder: A Critical Synthesis
Rajkumar, R. P. (2025) · Biomedicines · doi:10.3390/biomedicines13020507 · Cited by 2 · see citing works
Mattiolo, P., Γκουντάκος, Α., Centonze, G., Bevere, M., Piccoli, P., Ammendola, S., Pedrazzani, C., Landoni, L., Cingarlini, S., Milella, M., et al. (2023) · Pathology - Research and Practice · doi:10.1016/j.prp.2023.154674 · Cited by 2 · see citing works
Self-citationBeginning at the ends: telomere and telomere-based cancer therapeutics
Sadr, Z., Ghasemi, M., Jafarpour, S., Seyfi, R., Ghasemi, A., Boustanipour, E., Khorshid, H. R. K., & Ehtesham, N. (2024) · Molecular Genetics and Genomics · doi:10.1007/s00438-024-02206-6 · Cited by 1 · see citing works
Pérot, G., Guerriau, C., Roussel, N., Sarot, É., Valle, C., Pomiès, P., Tirode, F., Poncet, D., & Chibon, F. (2026) · BMC Cancer · doi:10.1186/s12885-026-16151-7 · Cited by 1 · see citing works
The Genomics of Liposarcoma: A Review and Commentary
Beird, H. C., Lazar, A. J., & Truong, D. D. (2022) · Global Journal of Human Social Science · doi:10.34257/gjsfrgvol22is2pg15 · Cited by 1 · see citing works
Bennett, D., Wierdl, M., Chakraborty, S., Johnson, J., Akingbehin, V., Estevez-Prado, D., Feng, Y., Morsby, J. J., Harper, J., Nezhady, M. A. M., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.04.709438 · Cited by 1 · see citing works
Clinical Relevance of Alternative Lengthening of Telomeres in Cancer
da Silva, G. G., Morais, K. S., Arcanjo, D. D. S., & de Oliveira, D. M. (2020) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026620666200110112854
Telomere Maintenance Mechanisms in Cancer
Jesus, T. T., Martins, R. S., Gaspar, T. B., Soares, P., & Vinagre, J. (2024) · Interdisciplinary cancer research · doi:10.1007/16833_2024_369
Farid, M., Chan, J. Y., Yang, V. S., Oh, B. L. Z., & Pang, A. S. L. (2025) · Springer eBooks · doi:10.1007/978-981-96-2163-7_9
Hosseini, S. A. M., Mahmoodieh, B., Hashemi, M., Asadifard, E., Hassanzadeh, F. G., Hassanzadeh, Z., Fazel, B., Hedayati, N., Hushmandi, K., Olianasab, S. A., et al. (2026) · Discover Oncology · doi:10.1007/s12672-026-04629-6
Biondi, N., Ratto, M. L., Pal, R., Rausch, T., Stirl, S., Villacorta, L., Hadzic, A., Knotz, C., Sieverling, L., González-Woge, M. A., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.17.725728
Jiménez-Ortega, R. F., Salgado, R. M., Rivera‐Paredez, B., Patiño, N., Hilario-Huerta, T., Arenas-Díaz, S., Velázquez‐Cruz, R., & Hidalgo‐Bravo, A. (2026) · Current Issues in Molecular Biology · doi:10.3390/cimb48060553
Folini, M., Pasquali, S., & Zaffaroni, N. (2026) · Research Square · doi:10.21203/rs.3.rs-11116403/v1
Lannoo, R., Bechter, O. E., & Daelemans, D. (2026) · Cancer Letters · doi:10.1016/j.canlet.2026.218888
- Authors
- Lawlor, R. T., Veronese, N., Pea, A., Nottegar, A., Smith, L., Pilati, C., Demurtas, J., Fassan, M., Cheng, L., & Luchini, C.
- Affiliations
- University of Verona (IT)
- National Research Council (IT)
- Ospedale San Bortolo (IT)
- Anglia Ruskin University (GB)
- Université Paris Descartes (FR)
- Corresponding author
- Luchini, Claudio
- ORCID
- Venue
- BMC Cancer
- Published
- 2019-03-14
- Volume
- 19
- Issue
- 1
- Pages
- 232-232
- ISSN
- 1471-2407 (ISSN-L)
- PMC
- PMC6419345
- OpenAlex
- W2933488927
- Cited by
- 62
- References
- 51
- Citations by year
- 2026: 9 · 2025: 7 · 2024: 8 · 2023: 9 · 2022: 7 · 2021: 8 · 2020: 9 · 2019: 5
- FWCI
- 0.85
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- BMC Cancer (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Nova Science Publishers (Nova Science Publishers, Inc.) (submittedVersion, other-oa)
- IUScholarWorks (Indiana University) (submittedVersion, cc-by)
- Purdue University Indianapolis (Indiana University) (submittedVersion, public-domain)
- Purdue University Indianapolis (Indiana University) (submittedVersion, cc-by)
- Padua Research Archive (University of Padova) (submittedVersion, cc-by)
- Funders
- Cassini Project 2017
- Fondazione Italiana per la Ricerca sul Cancro (12182)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Sarcoma Diagnosis and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- alternative lengthening of telomeres, soft tissue sarcoma, telomere maintenance, survival, mortality risk, prognostic factors, mitotic count, tumor grade
- MeSH terms
- Humans, Middle Aged, Prognosis, Sarcoma, Proportional Hazards Models, Survival Analysis, Telomere, Risk Assessment, Telomere Homeostasis
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