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Telomerase modulates Wnt signalling by association with target gene chromatin
Open accessAbstract
Stem cells are controlled, in part, by genetic pathways frequently dysregulated during human tumorigenesis. Either stimulation of Wnt/beta-catenin signalling or overexpression of telomerase is sufficient to activate quiescent epidermal stem cells in vivo, although the mechanisms by which telomerase exerts these effects are not understood. Here we show that telomerase directly modulates Wnt/beta-catenin signalling by serving as a cofactor in a beta-catenin transcriptional complex. The telomerase protein component TERT (telomerase reverse transcriptase) interacts with BRG1 (also called SMARCA4), a SWI/SNF-related chromatin remodelling protein, and activates Wnt-dependent reporters in cultured cells and in vivo. TERT serves an essential role in formation of the anterior-posterior axis in Xenopus laevis embryos, and this defect in Wnt signalling manifests as homeotic transformations in the vertebrae of Tert(-/-) mice. Chromatin immunoprecipitation of the endogenous TERT protein from mouse gastrointestinal tract shows that TERT physically occupies gene promoters of Wnt-dependent genes. These data reveal an unanticipated role for telomerase as a transcriptional modulator of the Wnt/beta-catenin signalling pathway.
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“As expected, AAV9-mTERT-DN treatment increased CyclinD1 expression in a number of tissues (Fig 5A and B), in accordance with previous findings (Park et al, 2009).”
From Telomerase gene therapy in adult and old mice delays aging and increases longevity without increasing cancer (2012) · cites this paper as Park et al, 2009
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“These results are consistent with previous findings that TERT can act as a transcriptional modulator not only in highly proliferating cells but also in terminally differentiated cells.16,27”
From TERT activation targets DNA methylation and multiple aging hallmarks (2024) · cites this paper as [27]
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“in agreement with the proposed role of TERT as activator of genes of the Wnt pathway (Park et al, 2009), tissues with increased TERT expression also showed increased expression of active β-catenin, as well as of its target gene cyclinD1, which in turn may mediate some of the known effects of TERT improving stem cell mobilization (Flores et al, 2005; Reya & Clevers, 2005; Sarin et al, 2005).”
From Telomerase gene therapy in adult and old mice delays aging and increases longevity without increasing cancer (2012) · cites this paper as Park et al, 2009
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“Stable overexpression of TERT in mouse skin enhanced the ability of bulge stem cells to enter cell cycle when stimulated with phorbol esters (147).”
From Telomeres and telomerase in cancer (2010) · cites this paper as [147]
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“The first connection between TERT and Wnt/ β-catenin pathway was discovered by Artandi’s group [89].”
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“Moreover, given the recent findings that Wnt signaling and the telomerase catalytic subunit (telomerase reverse transcriptase; TERT) can potentially make a positive regulatory loop: the Wnt pathway component β-catenin can positively regulate the expression of TERT while TERT can positively regulate the expression of W…”
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“…of this holoenzyme is an essential and limiting common denominator in the progression of ∼ 90% of human cancers including colorectal cancers (25–27). hTERT also has noncanonical roles in the regulation of inflammation and cancer (28) via activation of NF κ B (29), MYC (30), and WNT signaling (31).”
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“hTERT can also modulate Wnt/ -catenin signaling pathways by physically occupying the promoters of -catenin target genes to induce their transcription (8, 41).”
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“For instance, TERT is capable of regulating Wnt target genes by forming a transcriptional co-activation complex with β-catenin([66]).”
Zhang, X., Li, B., Yu, J., Dahlström, J., Tran, A. N., Björkholm, M., & Xu, D. (2018) · Annals of Hematology · doi:10.1007/s00277-018-3340-7 · Cited by 19
Chen, K.-H., Chen, L., Li, L., Qu, S., Yu, B., Sun, Y., Wan, F., Chen, X., Liang, R., & Zhu, X. (2020) · Journal of Cellular Biochemistry · doi:10.1002/jcb.29681 · Cited by 18
Ranches, G., Zeidler, M., Kessler, R., Hoelzl, M., Hess, M. W., Vosper, J., Perco, P., Schramek, H., Kummer, K. K., Kress, M., et al. (2022) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2022.04.035 · Cited by 18
Prasad, R. R., Mishra, D. K., Kumar, M., & Yadava, P. K. (2021) · Heliyon · doi:10.1016/j.heliyon.2021.e08673 · Cited by 19
“activates the Wnt/beta-catenin signaling and promotes the expression of growth controlling genes like EGFR, bFGF, and VEGF independent of telomerase activation [19, 20, 21].”
BackgroundVinayagamurthy, S., Bagri, S., Mergny, J., & Chowdhury, S. (2022) · Trends in Genetics · doi:10.1016/j.tig.2022.10.002 · Cited by 21
“TERT Cofactor of β-catenin transcriptional complex HeLa, mouse small intestine cells AXIN2, MYC, HPRT Cell proliferation, survival, and stemness [42]”
PinX1: a sought-after major tumor suppressor at human chromosome 8p23
Zhou, X. Z. (2011) · Oncotarget · doi:10.18632/oncotarget.339 · Cited by 18
“However, telomerase has other telomere-independent function such as in DNA damage response [95, 96] and activating β-catenin [97].”
Zhang, Y., Calado, R. T., Rao, M., Hong, J. A., Meeker, A. K., Dumitriu, B., Atay, S. M., McCormick, P. J., Garfield, S. H., Wangsa, D., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101010 · Cited by 18
“The fact that TERT not only interacts with and stabilizes bcatenin [23,54], but also is a direct target of b-catenin signaling [31,32], indicates that highly complex and interdependent regulatory networks mediate canonical and non-canonical telomerase activities in cancer cells.”
BackgroundSelf-citationOverexpression of Telomerase Reverse Transcriptase Induces Autism-like Excitatory Phenotypes in Mice
Kim, K. C., Rhee, J., Park, J., Lee, D.-K., Choi, C. S., Kim, J., Lee, H., Song, M.-R., Yoo, H. J., Chung, C., et al. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9630-3 · Cited by 18
“Chromatin immunoprecipitation (ChIP) using hTERTGFP overexpressed NPCs showed that TERT overexpression induced Brg1, β-catenin, and TERT protein binding to Pax6 gene promoter region (Fig.”
BackgroundInfluentialSelf-citation37 kDa LRP::FLAG enhances telomerase activity and reduces senescent markersin vitro
Otgaar, T. C., Ferreira, E., Malindisa, S. T., Bernert, M., Letsolo, B. T., & Weiss, S. F. T. (2017) · Oncotarget · doi:10.18632/oncotarget.21278 · Cited by 18
“A few of these include: DNA repair, cell proliferation, mtDNA protection as well as influencing a number of cellular pathways offering pro-proliferative functions [12, 13].”
BackgroundTelomerase Biogenesis and Activities from the Perspective of Its Direct Interacting Partners
Nguyen, K. T. T. T., & Wong, J. M. Y. (2020) · Cancers · doi:10.3390/cancers12061679 · Cited by 18
“Th TERT-BRG1 complex in turn promotes transcription of Wnt-dependent genes, including c-MYC and cyclin D1, by physically ccupying their promoter regions [103].”
BackgroundInfluentialClonal inactivation of TERT impairs stem cell competition
Hasegawa, K., Zhao, Y., Garbuzov, A., Corces, M. R., Neuhöfer, P., Gillespie, V. M., Cheung, P., Belk, J. A., Huang, Y., Wei, Y., et al. (2024) · Nature · doi:10.1038/s41586-024-07700-w · Cited by 20
Self-citationGenetic and epigenetic trends in telomere research: a novel way in immunoepigenetics
Melicher, D., Buzás, E. I., & Falus, A. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1991-2 · Cited by 17
Telomerase reverse transcriptase catalytic subunit expression and proliferation index in Wilms tumor
Dınız, G., Aktaş, S., Yıldırım, A. T., Temir, G., Ortaç, R., & Vergin, C. R. (2011) · Tumor Biology · doi:10.1007/s13277-011-0178-1 · Cited by 17
Wang, F., Fu, P., Pang, Y., Liu, C., Shao, Z., Zhu, J., Li, J., Wang, T., Zhang, X., & Liu, J. (2014) · Tumor Biology · doi:10.1007/s13277-014-1611-z · Cited by 17
“These functions include regulation of gene expression [3–5] and modulation of cellular signaling [6, 7] or cell cycle regulation [8], protection of mitochondria and mtDNA [9], inhibition of apoptosis [10, 11], and modulation of DNA damage response [12].”
BackgroundTelomerase Reverse Transcriptase Has an Extratelomeric Function in Somatic Cell Reprogramming
Kinoshita, T., Nagamatsu, G., Saito, S., Takubo, K., Horimoto, K., & Suda, T. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.536037 · Cited by 19
“In addition to telomere elongation, TERT has other functions, including RNA-dependent RNA polymerase activity and modulation of -catenin signaling (31, 32).”
BackgroundHeterogeneity in readouts of canonical wnt pathway activity within intestinal crypts
Li, N., Yousefi, M., Nakauka‐Ddamba, A., Tobias, J. W., Jensen, S. T., Morrisey, E. E., & Lengner, C. J. (2016) · Developmental Dynamics · doi:10.1002/dvdy.24423 · Cited by 17
“Similarly, it appears that the widely used Axin2-LacZ allele does not label Paneth cells either, although the diffuse nature of X-gal staining make interpretation of Axin2-LacZ expression at the single cell level challenging (Lustig et al., 2002; Park et al., 2009; Johnson et al., 2013).”
Wu, Y., Zhong, D., Li, Y., Wu, H., Xu, X., Yang, J., & Gu, Z. (2020) · Advanced Healthcare Materials · doi:10.1002/adhm.201901739 · Cited by 17
Telomerase RNA recruits RNA polymerase II to target gene promoters to enhance myelopoiesis
García‐Castillo, J., Alcaraz‐Pérez, F., Martínez‐Balsalobre, E., García‐Moreno, D., Rossmann, M. P., Fernández-Lajarín, M., Bernabé‐García, M., Pérez‐Oliva, A. B., Rodríguez-Cortez, V., Bueno, C., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2015528118 · Cited by 17
The Relevance of Telomerase and Telomere-Associated Proteins in B-Acute Lymphoblastic Leukemia
da Mota, T. H. A., Camargo, R., Biojone, E. R., Guimarães, A. F. R., Pittella-Silva, F., & de Oliveira, D. M. (2023) · Genes · doi:10.3390/genes14030691 · Cited by 16
Hill, C., Duffy, S., Kettyle, L. M., McGlynn, L. M., Sandholm, N., Salem, R. M., Thompson, A., Swan, E. J., Kilner, J., Rossing, P. R., et al. (2023) · Genes · doi:10.3390/genes14051029 · Cited by 15
“controlling proliferation independent of TERT catalytic activity or the telomerase RNA component (TERC) [103,106,107].”
InfluentialTERT Expression Induces Resistance to BRAF and MEK Inhibitors in BRAF-Mutated Melanoma In Vitro
Delyon, J., Vallet, A., Bernard-Cacciarella, M., Kuzniak, I., de Moura, C. R., Louveau, B., Jouenne, F., Mourah, S., Lebbé, C., & Dumaz, N. (2023) · Cancers · doi:10.3390/cancers15112888 · Cited by 15
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
Amjadi‐Moheb, F., Paniri, A., & Akhavan‐Niaki, H. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-3613 · Cited by 16
“Furthermore, the application of chromatin isolation by RNA purification (ChIRP) to define the genomic interactions of lncRNAs, has identified the TERC occupancy at the MYC promoter probably through a cytosine-rich sequence motif (154, 155).”
BackgroundPortrait of replication stress viewed from telomeres
Ishikawa, F. (2013) · Cancer Science · doi:10.1111/cas.12165 · Cited by 18
Wang, K., Jiang, S., Huang, A., Gao, Y., Peng, B., Li, Z., Ma, W., Songyang, Z., Zhang, S., He, M., et al. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.575358 · Cited by 16
“has disclosed that hTERT is significantly related to cyclin D1 expression (43).”
BackgroundTelomeres, a busy platform for cell signaling.
Gardano, L., Pucci, F., Christian, L., Le Bihan, T., & Harrington, L. (2013) · Frontiers in Oncology · doi:10.3389/fonc.2013.00146 · Cited by 15
“…previous finding of complexes containing both telomerase and β-catenin at promoter sequences show that β-catenin and telomere integrity are Frontiers in Oncology | Cancer Molecular Targets and Therapeutics June 2013 | Volume 3 | Article 146 | 8 connected (Park et al., 2009; Hoffmeyer et al., 2012).”
BackgroundInfluentialEndorf, E. B., 青华, Aono, J., Terami, N., Doyon, G., Hyzny, E. J., Jones, K. L., Findeisen, H. M., & Bruemmer, D. (2016) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.116.308717 · Cited by 15
Metadata
- Authors
- Park, J.-I., Venteicher, A. S., Hong, J. Y., Choi, J., Jun, S., Shkreli, M., Chang, W., Meng, Z., Cheung, P., Ji, H., McLaughlin, M., Veenstra, T. D., Nusse, R., McCrea, P. D., & Artandi, S. E.
- Affiliations
- Stanford Medicine (US)
- The University of Texas MD Anderson Cancer Center (US)
- National Cancer Institute (US)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Artandi, Steven E.
- ORCID
- Venue
- Nature
- Published
- 2009-07
- Volume
- 460
- Issue
- 7251
- Pages
- 66-72
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4349391
- OpenAlex
- W2086316954
- Cited by
- 707
- References
- 51
- Citations by year
- 2026: 17 · 2025: 28 · 2024: 23 · 2023: 41 · 2022: 32 · 2021: 48 · 2020: 48 · 2019: 34 · 2018: 38 · 2017: 29 · 2016: 43 · 2015: 48 · 2014: 58 · 2013: 58 · 2012: 60
- FWCI
- 21.63
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DigitalCommons-Cedarville (Cedarville University) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Cancer Institute (CA111691, R01CA125453, CA125453, R01CA111691, P30CA124435)
- National Institute of General Medical Sciences (R01GM052112)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- telomerase, telomerase reverse transcriptase, Wnt/β-catenin signaling, SMARCA4, chromatin remodeling, transcriptional regulation, epidermal stem cells, stem cell self-renewal, carcinogenesis, anterior-posterior axis, homeotic transformation, promoter, SWI/SNF complex
- MeSH terms
- Animals, Cell Line, Choristoma, Chromatin, DNA Helicases, HeLa Cells, Humans, Intestine, Small, Nuclear Proteins, Oocytes, Plasmids, Promoter Regions, Genetic, Transcription Factors, Xenopus laevis, Signal Transduction, Genes, Reporter, Telomerase, Somites, Wnt Proteins, beta Catenin, Mice, Wnt3 Protein
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