Telomerase and cancer therapeutics

Harley, Calvin B.

doi:10.1038/nrc2275

Cited by 734Telomeres, Telomerase, and SenescenceImmunotherapy and Immune ResponsesVirus-based gene therapy research

Telomerase and cancer therapeutics

Harley, Calvin B.·2008·Nature Reviews Cancer

DOI 10.1038/nrc2275

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Abstract

Telomerase is an attractive cancer target as it appears to be required in essentially all tumours for immortalization of a subset of cells, including cancer stem cells. Moreover, differences in telomerase expression, telomere length and cell kinetics between normal and tumour tissues suggest that targeting telomerase would be relatively safe. Clinical trials are ongoing with a potent and specific telomerase inhibitor, GRN163L, and with several versions of telomerase therapeutic vaccines. The prospect of adding telomerase-based therapies to the growing list of new anticancer products is promising, but what are the advantages and limitations of different approaches, and which patients are the most likely to respond?

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The demonstration that dysfunctional telomeres could engage a senescence program to suppress tumorigenesis in vivo suggests possible future therapeutic applications.
“The demonstration that dysfunctional telomeres could engage a senescence program to suppress tumorigenesis in vivo suggests possible future therapeutic applications63.”
From Telomere dysfunction and tumour suppression: the senescence connection (2008) · cites this paper as [63]

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Damle, R. N., Batliwalla, F., Ghiotto, F., Valetto, A., Albesiano, E., Sison, C. P., Allen, S. L., Kolitz, J. E., Vinciguerra, V. P., Kudalkar, P., et al. (2003) · Blood · doi:10.1182/blood-2003-04-1345 · Cited by 181 · see citing works
Telomerase Activity Concentrates in the Mitotically Active Segments of Human Hair Follicles
Ramirez, R. D., Wright, W. E., Shay, J. W., & Taylor, R. S. (1997) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12285654 · Cited by 174 · see citing works
Disruption of Telomere Maintenance by Depletion of the MRE11/RAD50/NBS1 Complex in Cells That Use Alternative Lengthening of Telomeres
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
Cellular and Gene Expression Responses Involved in the Rapid Growth Inhibition of Human Cancer Cells by RNA Interference-mediated Depletion of Telomerase RNA
Li, S., Crothers, J., Haqq, C. M., & Blackburn, E. H. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502782200 · Cited by 158 · see citing works
Induction of Ovarian Cancer Cell Apoptosis by 1,25-Dihydroxyvitamin D3 through the Down-regulation of Telomerase
Jiang, F., Bao, J., Li, P., Nicosia, S. V., & Bai, W. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m410395200 · Cited by 153 · see citing works
Telomerase Antagonists GRN163 and GRN163L Inhibit Tumor Growth and Increase Chemosensitivity of Human Hepatoma *
Djojosubroto, M. W., Chin, A. C., Go, N., Schaetzlein, S., Manns, M. P., Gryaznov, S., Harley, C. B., & Rudolph, L. K. (2005) · Hepatology · doi:10.1002/hep.20822 · Cited by 151 · see citing works
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Developmental regulation of telomerase activity in human fetal tissues during gestation
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Telomerase Template Antagonist GRN163L Disrupts Telomere Maintenance, Tumor Growth, and Metastasis of Breast Cancer
Hochreiter, A. E., Xiao, H., Goldblatt, E. M., Gryaznov, S. M., Miller, K. D., Badve, S., Sledge, G. W., & Herbert, B.-S. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-2760 · Cited by 146 · see citing works
Targeting the Limitless Replicative Potential of Cancer: The Telomerase/Telomere Pathway
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Mechanism of acridine-based telomerase inhibition and telomere shortening
Gunaratnam, M., Greciano, O., Martins, C., Reszka, A. P., Schultes, C. M., Morjani, H., Riou, J., & Neidle, S. (2007) · Biochemical Pharmacology · doi:10.1016/j.bcp.2007.06.011 · Cited by 139 · see citing works
Telomerase levels control the lifespan of human T lymphocytes
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Effects of a novel telomerase inhibitor, GRN163L, in human breast cancer
Gellert, G. C., Dikmen, Z. G., Wright, W. E., Gryaznov, S. M., & Shay, J. W. (2005) · Breast Cancer Research and Treatment · doi:10.1007/s10549-005-9043-5 · Cited by 126 · see citing works
Pattern abnormalities induced by ectopic expression of the Drosophila gene hairy are associated with repression of ftz transcription
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Human Cancer Cells Harbor T-Stumps, a Distinct Class of Extremely Short Telomeres
Xu, L., & Blackburn, E. H. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.10.005 · Cited by 121 · see citing works
Enhanced induction of telomerase-specific CD4(+) T cells using dendritic cells transfected with RNA encoding a chimeric gene product.
Su, Z. Z., Vieweg, J., Weizer, A. Z., Dahm, P., Yancey, D. R., Turaga, V., Higgins, J., Boczkowski, D., Gilboa, E., & Dannull, J. (2002) · PubMed · Cited by 117 · see citing works
Immunization of Patients with the hTERT:540-548 Peptide Induces Peptide-Reactive T Lymphocytes That Do Not Recognize Tumors Endogenously Expressing Telomerase
Parkhurst, M. R., Riley, J. P., Igarashi, T., Li, Y., Robbins, P. F., & Rosenberg, S. A. (2004) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-0325 · Cited by 111 · see citing works
Vaccination of Patients With Advanced Non–Small-Cell Lung Cancer With an Optimized Cryptic Human Telomerase Reverse Transcriptase Peptide
Bolonaki, I., Kotsakis, A. P., Papadimitraki, E., Aggouraki, D., Konsolakis, G., Vagia, A., Christophyllakis, C., Nikoloudi, I., Magganas, E., Galanis, A., et al. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2006.10.3465 · Cited by 108 · see citing works
Ex Vivo Characterization of Multiepitopic Tumor-Specific CD8 T Cells in Patients with Chronic Myeloid Leukemia: Implications for Vaccine Development and Adoptive Cellular Immunotherapy
Gannagé, M., Abel, M., Michallet, A., Delluc, S., Lambert, M., Giraudier, S., Kratzer, R., Niedermann, G., Saveanu, L., Guilhot, F., et al. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.12.8210 · Cited by 106 · see citing works
Telomere Biology and Cellular Aging in Nonhuman Primate Cells
Steinert, S., White, D. M., Zou, Y. S., Shay, J. W., & Wright, W. E. (2002) · Experimental Cell Research · doi:10.1006/excr.2001.5409 · Cited by 99 · see citing works
Pharmacological Telomerase Inhibition Can Sensitize Drug-Resistant and Drug-Sensitive Cells to Chemotherapeutic Treatment
Ward, R. J., & Autexier, C. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.011494 · Cited by 99 · see citing works
Telomerase-Specific T-Cell Immunity in Breast Cancer: Effect of Vaccination on Tumor Immunosurveillance
Domchek, S. M., Recio, A., Mick, R., Clark, C. E., Carpenter, E. L., Fox, K. R., DeMichele, A. M., Schuchter, L. M., Leibowitz, M. S., Wexler, M. H., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-2765 · Cited by 99 · see citing works
Ribozyme-mediated telomerase inhibition induces immediate cell loss but not telomere shortening in ovarian cancer cells
Saretzki, G. C., Ludwig, A., von Zglinicki, T., & Runnebaum, I. B. (2001) · Cancer Gene Therapy · doi:10.1038/sj.cgt.7700383 · Cited by 98 · see citing works
Telomerase activity and telomere length in pediatric patients with malignancies undergoing chemotherapy
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Preferential maintenance of critically short telomeres in mammalian cells heterozygous for mTert
Liu, Y., Kha, H. T., Ungrin, M., Robinson, M. O., & Harrington, L. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.062549199 · Cited by 94 · see citing works
Telomerase and its potential for therapeutic intervention
Phatak, P., & Burger, A. M. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707374 · Cited by 90 · see citing works
Conditionally replicative adenovirus driven by the human telomerase promoter provides broad-spectrum antitumor activity without liver toxicity
Irving, J., Wang, Z., Powell, S., O’Sullivan, C., Mok, M. T. C., Murphy, B., Cardoza, L. M., LEBKOWSKI, J. S., & Majumdar, A. S. (2004) · Cancer Gene Therapy · doi:10.1038/sj.cgt.7700666 · Cited by 87 · see citing works
Telomerase inhibition with an oligonucleotide telomerase template antagonist: in vitro and in vivo studies in multiple myeloma and lymphoma
Wang, E. S., Wu, K., Chin, A. C., Chen‐Kiang, S., Pongracz, K., Gryaznov, S. M., & Moore, M. A. S. (2003) · Blood · doi:10.1182/blood-2003-02-0546 · Cited by 83 · see citing works
Telomerase induction in T cells: A cure for aging and disease?
Effros, R. B. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.11.005 · Cited by 82 · see citing works
Selective ablation of human cancer cells by telomerase-specific adenoviral suicide gene therapy vectors expressing bacterial nitroreductase
Bilsland, A. E., Anderson, C. J., Fletcher‐Monaghan, A. J., McGregor, F., Evans, T. R. J., Ganly, I., Knox, R. J., Plumb, J. A., & Keith, W. N. (2003) · Oncogene · doi:10.1038/sj.onc.1206168 · Cited by 79 · see citing works
Equivalent induction of telomerase-specific cytotoxic T lymphocytes from tumor-bearing patients and healthy individuals.
Vonderheide, R. H., Schultze, J. L., Anderson, K. S., Maecker‐Kolhoff, B., Butler, M. O., Xia, Z., Kuroda, M. J., von Bergwelt‐Baildon, M. S., Bedor, M., Hoar, K. M., et al. (2001) · PubMed · Cited by 77 · see citing works
Idiopathic Pulmonary Fibrosis — New Insights
Verma, S., & Slutsky, A. S. (2007) · New England Journal of Medicine · doi:10.1056/nejmcibr070490 · Cited by 76 · see citing works
Telomerase and Cancer Stem CellsPreprint
Armanios, M. Y., & Greider, C. W. (2005) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2005.70.030 · Cited by 76 · see citing works
Specific telomere dysfunction induced by GRN163L increases radiation sensitivity in breast cancer cells
Gómez‐Millán, J., Goldblatt, E. M., Gryaznov, S. M., Mendonca, M. S., & Herbert, B. (2006) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2006.09.038 · Cited by 72 · see citing works
Antiadhesive Effects of GRN163L—An Oligonucleotide N3′→P5′ Thio-Phosphoramidate Targeting Telomerase
Jackson, S. R., Zhu, C.-H., Paulson, V., Watkins, L., Dikmen, Z. G., Gryaznov, S. M., Wright, W. E., & Shay, J. W. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-2306 · Cited by 72 · see citing works
Telomeres and telomerase as targets for cancer therapy
Zimmermann, S., & Martens, U. M. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-6481-8 · Cited by 62 · see citing works
Human Is a Unique Species among Primates in Terms of Telomere Length
Kakuo, S., Asaoka, K., & Ide, T. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.1385 · Cited by 60 · see citing works
Generation of Telomeric G Strand Overhangs Involves Both G and C Strand Cleavage
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Frequency of telomerase-specific CD8+ T lymphocytes in patients with cancer
Filaci, G., Fravega, M., Setti, M., Traverso, P., Millo, E., Fenoglio, D., Negrini, S. M., Ferrera, F., Romagnoli, A., Basso, M., et al. (2005) · Blood · doi:10.1182/blood-2005-01-0258 · Cited by 57 · see citing works
Antitumor effects of specific telomerase inhibitor GRN163 in human glioblastoma xenografts
Ozawa, T., Gryaznov, S. M., Hu, L. J., Pongracz, K., Santos, R. A., Bollen, A. W., Lamborn, K. R., & Deen, D. F. (2004) · Neuro-Oncology · doi:10.1215/s1152851704000055 · Cited by 56 · see citing works
Interaction of Human Telomerase with Its Primer Substrate
Wallweber, G. J., Gryaznov, S. M., Pongracz, K., & Pruzan, R. (2002) · Biochemistry · doi:10.1021/bi026914a · Cited by 55 · see citing works
Association between telomere length and VH gene mutation status in chronic lymphocytic leukaemia: clinical and biological implications
Hultdin, M., Rosenquist, R., Thunberg, U., Tobin, G., Norrback, K.-F., Johnson, A., Sundström, C., & Roos, G. (2003) · British Journal of Cancer · doi:10.1038/sj.bjc.6600763 · Cited by 55 · see citing works
A Phase I Study of the Optimized Cryptic Peptide TERT572Y in Patients with Advanced Malignancies
Mavroudis, D., Bolonakis, I., Cornet, S., Myllaki, G., Kanellou, P., Kotsakis, A. P., Galanis, A., Nikoloudi, I., Spyropoulou, M., Menez, J., et al. (2006) · Oncology · doi:10.1159/000096252 · Cited by 55 · see citing works
Telomere dynamics in human cells
Baird, D. M. (2007) · Biochimie · doi:10.1016/j.biochi.2007.08.003 · Cited by 54 · see citing works
Inhibition of telomerase by BIBR 1532 and related analogues
Barma, D. K., Elayadi, A. N., Falck, J. R., & Corey, D. R. (2003) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/s0960-894x(03)00101-x · Cited by 52 · see citing works
Telomerase Activity in Bovine Embryos During Early Development1
Xu, J., & Yang, X. (2000) · Biology of Reproduction · doi:10.1095/biolreprod63.4.1124 · Cited by 52 · see citing works
Ink4a / Arf tumor suppressor does not modulate the degenerative conditions or tumor spectrum of the telomerase-deficient mouse
Khoo, C. M., Carrasco, D. R., Bosenberg, M. W., Paik, J.-H., & DePinho, R. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700093104 · Cited by 52 · see citing works
Telomerase Therapeutics for Degenerative Diseases
Harley, C. B. (2005) · Current Molecular Medicine · doi:10.2174/1566524053586671 · Cited by 51 · see citing works
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Early hematopoietic reconstitution after clinical stem cell transplantation: evidence for stochastic stem cell behavior and limited acceleration in telomere loss
Thornley, I., Sutherland, R., Wynn, R. F., Nayar, R., Sung, L., Corpus, G., Kiss, T. L., Lipton, J. H., Doyle, J., Saunders, F., et al. (2002) · Blood · doi:10.1182/blood.v99.7.2387 · Cited by 51 · see citing works
Dyskeratosis Congenita: A Disorder of Defective Telomere Maintenance?
Walne, A. J., Marrone, A., & Dokal, I. S. (2005) · International Journal of Hematology · doi:10.1532/ijh97.05067 · Cited by 50 · see citing works
Increased Safety with Preserved Antitumoral Efficacy on Hepatocellular Carcinoma with Dual-Regulated Oncolytic Adenovirus
Zhang, Q., Chen, G., Peng, L., Wang, X., Yang, Y., Liu, C., Shi, W., Su, C., Wu, H., Liu, X., et al. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-1491 · Cited by 48 · see citing works
Drug Insight: cancer cell immortality—telomerase as a target for novel cancer gene therapies
Keith, W. N., Bilsland, A. E., Hardie, M., & Evans, T. J. (2004) · Nature Clinical Practice Oncology · doi:10.1038/ncponc0044 · Cited by 44 · see citing works
Telomere dynamics in childhood leukemia and solid tumors: a follow-up study
Franco, S., Ozkaynak, M. F., Sandoval, C., Tugal, O., Jayabose, S., Engelhardt, M. M., & Moore, M. A. S. (2003) · Leukemia · doi:10.1038/sj.leu.2402815 · Cited by 43 · see citing works
Telomerase immunity from bench to bedside: round one
Cortez-Gonzalez, X., & Zanetti, M. (2007) · Journal of Translational Medicine · doi:10.1186/1479-5876-5-12 · Cited by 43 · see citing works
Assembly of Mutant-Template Telomerase RNA into Catalytically Active Telomerase Ribonucleoprotein That Can Act on Telomeres Is Required for Apoptosis and Cell Cycle Arrest in Human Cancer Cells
Goldkorn, A., & Blackburn, E. H. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3782 · Cited by 42 · see citing works
The Role of Surgery in N2 Non–Small Cell Lung Cancer
DeCamp, M. M., Ashiku, S. K., & Thurer, R. L. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-9013 · Cited by 42 · see citing works
Telomerase vaccination has no detectable effect on SCID-repopulating and colony-forming activities in the bone marrow of cancer patients
Danet-Desnoyers, G.-A., Luongo, J. L., Bonnet, D. A., Domchek, S. M., & Vonderheide, R. H. (2005) · Experimental Hematology · doi:10.1016/j.exphem.2005.07.011 · Cited by 41 · see citing works
Telomerase targeted oligonucleotide thio‐phosphoramidates in T24‐luc bladder cancer cells
Dikmen, Z. G., Wright, W. E., Shay, J. W., & Gryaznov, S. M. (2007) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21635 · Cited by 40 · see citing works
Benefits of bad telomeres
Hanahan, D. (2000) · Nature · doi:10.1038/35020662 · Cited by 39 · see citing works
Short telomeres and high telomerase activity in T-cell prolymphocytic leukemia
Röth, A., Dürig, J., Himmelreich, H., Bug, S., Siebert, R., Dührsen, U., Lansdorp, P. M., & Baerlocher, G. M. (2007) · Leukemia · doi:10.1038/sj.leu.2404968 · Cited by 33 · see citing works
Marked telomere shortening in mobilized peripheral blood progenitor cells (PBPC) following two tightly spaced high-dose chemotherapy courses with G-CSF
Ricca, I., Compagno, M., Ladetto, M., Rocci, A., Dell'Aquila, M., Omedè, P., Marco, F. D., D’Antico, S., Caracciolo, D., Ferrero, D., et al. (2005) · Leukemia · doi:10.1038/sj.leu.2403652 · Cited by 29 · see citing works
Optimization of the TRAP assay to evaluate specificity of telomerase inhibitors
Piotrowska, K., Kleideiter, E., Mürdter, T. E., Taetz, S., Baldes, C., Schaefer, U. F., Lehr, C., & Klotz, U. E. (2005) · Laboratory Investigation · doi:10.1038/labinvest.3700352 · Cited by 28 · see citing works
GV-1001, an injectable telomerase peptide vaccine for the treatment of solid cancers.
Nava-Parada, P., & Emens, L. A. (2007) · PubMed · Cited by 28 · see citing works
Magnetic resonance imaging in cardiology
Rademakers, F. E. (2003) · The Lancet · doi:10.1016/s0140-6736(03)12440-3 · Cited by 24 · see citing works
Harnessing Telomerase in Cancer Therapeutics
Fakhoury, J. J., Nimmo, G. A. M., & Autexier, C. (2007) · Anti-Cancer Agents in Medicinal Chemistry · doi:10.2174/187152007781058622 · Cited by 24 · see citing works
Phase I study of transgenic B lymphocyte immunization (TLI) against telomerase in androgen-independent prostate cancer (PC)
Millard, F. E., Gerloni, M., Darrah, D. D., Farness, P., & Zanetti, M. (2004) · Journal of Clinical Oncology · doi:10.1200/jco.2004.22.90140.2519 · Cited by 9 · see citing works
Telomerase activity in human germline and embryonic tissues and cells
Wright, W. E., Piatyszek, M. A., Rainey, W. E., Byrd, W., & Shay, J. W. (1996) · Developmental Genetics · doi:10.1002/(sici)1520-6408(1996)18:2

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Principles of cancer therapy: oncogene and non-oncogene addiction
Luo, J., Solimini, N. L., & Elledge, S. J. (2009) · Cell · doi:10.1016/j.cell.2009.02.024 · Cited by 1,765 · see citing works
Nanomedicine Applications of Hybrid Nanomaterials Built from Metal–Ligand Coordination Bonds: Nanoscale Metal–Organic Frameworks and Nanoscale Coordination Polymers
He, C., Liu, D., & Lin, W. (2015) · Chemical Reviews · doi:10.1021/acs.chemrev.5b00125 · Cited by 1,006 · see citing works
Untitled work
Wang (2012) · doi:10.1161/circresaha.111.261388 · Cited by 957 · see citing works
Trans-ancestry mutational landscape of hepatocellular carcinoma genomes
Totoki, Y., Tatsuno, K., Covington, K. R., Ueda, H., Creighton, C. J., Kato, M., Tsuji, S., Donehower, L. A., Slagle, B. L., Nakamura, H., et al. (2014) · Nature Genetics · doi:10.1038/ng.3126 · Cited by 781 · see citing works
Role of Telomeres and Telomerase in Aging and Cancer
Shay, J. W. (2016) · Cancer Discovery · doi:10.1158/2159-8290.cd-16-0062 · Cited by 668 · see citing works
Telomeric and extra-telomeric roles for telomerase and the telomere-binding proteins
Martínez, P., & Blasco, M. A. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3025 · Cited by 530 · see citing works
Silencing disease genes in the laboratory and the clinic
Watts, J. K., & Corey, D. R. (2011) · The Journal of Pathology · doi:10.1002/path.2993 · Cited by 472 · see citing works
Pro-senescence therapy for cancer treatment
Nardella, C., Clohessy, J. G., Alimonti, A., & Pandolfi, P. P. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3057 · Cited by 437 · see citing works
A systematic review of the anticancer properties of berberine, a natural product from Chinese herbs
Sun, Y., Xun, K., Wang, Y., & Chen, X. (2009) · Anti-Cancer Drugs · doi:10.1097/cad.0b013e328330d95b · Cited by 418 · see citing works
Telomere dysfunction and tumour suppression: the senescence connection
Deng, Y., Chan, S. S., & Chang, S. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2393 · Cited by 411 · see citing works
Telomerase directly regulates NF-κB-dependent transcription
Ghosh, A., Saginc, G., Leow, S. C., Khattar, E., Shin, E. M., Yan, T. D., Wong, M., Zhang, Z., Li, G., Sung, W.-K., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2621 · Cited by 378 · see citing works
The roles of senescence and telomere shortening in cardiovascular disease
Fyhrquist, F., Saijonmaa, O. J., & Strandberg, T. E. (2013) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2013.30 · Cited by 368 · see citing works
A mechanistic classification of clinical phenotypes in neuroblastoma
Ackermann, S., Cartolano, M., Hero, B., Welte, A., Kahlert, Y., Roderwieser, A., Bartenhagen, C., Walter, E., Gecht, J., Kerschke, L., et al. (2018) · Science · doi:10.1126/science.aat6768 · Cited by 338 · see citing works
Telomerase: An RNP Enzyme Synthesizes DNAPreprint
Blackburn, E. H., & Collins, K. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a003558 · Cited by 333 · see citing works
Deubiquitinases in cancer
Dewson, G., Eichhorn, P. J. A., & Komander, D. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00633-y · Cited by 337 · see citing works
DNAzyme-Based Biosensors: Immobilization Strategies, Applications, and Future Prospective
Khan, S. A., Burciu, B., Filipe, C. D. M., Li, Y., Dellinger, K., & Didar, T. F. (2021) · ACS Nano · doi:10.1021/acsnano.1c04327 · Cited by 329 · see citing works
Chemistry in human telomere biology: structure, function and targeting of telomere DNA/RNA
Xu, Y. (2011) · Chemical Society Reviews · doi:10.1039/c0cs00134a · Cited by 322 · see citing works
Novel anticancer therapeutics targeting telomerase
Ruden, M., & Puri, N. (2012) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2012.06.007 · Cited by 309 · see citing works
Designing a broad-spectrum integrative approach for cancer prevention and treatment
Block, K. I., Gyllenhaal, C., Lowe, L. J., Amedei, A., Amin, A. R. M. R., Amin, A., Aquilano, K., Arbiser, J. L., Arreola, A., Arzumanyan, A. L., et al. (2015) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2015.09.007 · Cited by 303 · see citing works
Rationally Engineered Nucleic Acid Architectures for Biosensing Applications
Xiao, M., Lai, W., Man, T., Chang, B., Li, L., Chandrasekaran, A. R., & Pei, H. (2019) · Chemical Reviews · doi:10.1021/acs.chemrev.9b00121 · Cited by 289 · see citing works
Telomerase reverse transcriptase promotes epithelial-mesenchymal transition and stem cell-like traits in cancer cells
Liu, Z., Li, Q., Li, K., Chen, L., Li, W., Hou, M., Liu, T., Yang, J., Lindvall, C., Björkholm, M., et al. (2013) · Oncogene · doi:10.1038/onc.2012.441 · Cited by 276 · see citing works
Telomere-driven diseases and telomere-targeting therapies
Martínez, P., & Blasco, M. A. (2017) · Journal of Cell Biology · doi:10.1083/jcb.201610111 · Cited by 257 · see citing works
“Telomeres as therapeutic targets • martínez and Blasco 883 notherapy, gene therapy using telomerase promoter-driven expression of a suicide gene, and chemicals that block telomerase biogenesis (Harley, 2008; Agrawal et al., 2012; Buseman et al., 2012; Jafri et al., 2016).”
Background
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
The role of telomeres and telomerase in cirrhosis and liver cancer
Nault, J., Ningarhari, M., Rebouissou, S., & Zucman‐Rossi, J. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0165-3 · Cited by 241 · see citing works
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Authors: Harley, C. B.
Affiliations: Geron (United States) (US)
Corresponding author: Harley, Calvin B.
Venue: Nature Reviews Cancer
Publisher: Springer Science and Business Media LLC
Published: 2008-03
Volume: 8
Issue: 3
Pages: 167-179
ISSN: 1474-175X (ISSN-L)
1474-1768
DOI: 10.1038/nrc2275
OpenAlex: W2078805336
Cited by: 728
References: 147
Citations by year: 2026: 11 · 2025: 22 · 2024: 26 · 2023: 39 · 2022: 20 · 2021: 29 · 2020: 38 · 2019: 39 · 2018: 27 · 2017: 38 · 2016: 48 · 2015: 58 · 2014: 48 · 2013: 51 · 2012: 53
FWCI: 6.57
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Cancer (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
Keywords: telomerase, telomerase inhibitors, GRN163L, cancer therapeutics, cancer stem cells, telomere length, cell kinetics, anticancer drug development
MeSH terms: Antineoplastic Agents, Clinical Trials as Topic, Enzyme Inhibitors, Humans, Immunotherapy, Kinetics, Medical Oncology, Models, Biological, Neoplasms, Oligonucleotides, Oligopeptides, Gene Expression Regulation, Neoplastic, Telomerase, Cancer Vaccines

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