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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Stable TERT overexpression in mouse skin enhanced bulge stem cell entry into cell cycle after phorbol ester stimulation.
“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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“Most likely, telomerase is primarily required to directly act on chromosome ends in hematopoietic cells themselves, however secondary, indirect effects of telomerase via cells that support cell proliferation [29] or possible effects of the TERT protein on transcription in stem cells [30] are difficult to exclude.”
BackgroundA central role for cadherin signaling in cancer
Kourtidis, A., Lu, R., Pence, L. J., & Anastasiadis, P. Z. (2017) · Experimental Cell Research · doi:10.1016/j.yexcr.2017.04.006 · Cited by 251 · see citing works
Transcriptional Regulation of Wnt/β-Catenin Pathway in Colorectal Cancer
Bian, J., Dannappel, M., Wan, C., & Firestein, R. (2020) · Cells · doi:10.3390/cells9092125 · Cited by 254 · see citing works
“Remarkably, telomerase and Wnt/β-catenin pathway can also converge, via the association between TERT and BRG1, to synergistically mediate stem cell development [203].”
BackgroundTelomerase at the intersection of cancer and aging
de Jesus, B. B., & Blasco, M. A. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.06.007 · Cited by 251 · see citing works
“In addition to the canonical role of telomerase in maintaining telomeres above a critical length, telomerase has also been proposed to regulate other pathways, which could have an impact on cancer growth, such as regulation of Wnt targets and metabolism (82, 96).”
Liu, T., Wang, N., Cao, J., Sofiadis, A., Dinets, A., Zedenius, J., Larsson, C., & Xu, D. (2013) · Oncogene · doi:10.1038/onc.2013.446 · Cited by 251 · see citing works
The role of telomeres and telomerase in cirrhosis and liver cancer
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Wnt signaling in stem and cancer stem cells
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Telomere-independent Rap1 is an IKK adaptor and regulates NF-κB-dependent gene expression
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Reactivation of telomerase in cancer
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“Although the major function of telomerase is thought to be telomere elongation, accumulating evidence has suggested that it can modulate expression of various genes including target of Wnt/b-catenin [44] and NFjB signaling [42] which affect cancer progression and tumorigenesis [45].”
BackgroundWnt/beta-Catenin Signaling and Small Molecule Inhibitors
Voronkov, A. E., & Krauss, S. J. K. (2012) · Current Pharmaceutical Design · doi:10.2174/138161213804581837 · Cited by 224 · see citing works
“One of them is TERT (telomerase reverse transcriptase), a catalytic subunit of telomerase, that was shown to directly regulate Wnt/ -catenin signal by participating as a co-factor in the -catenin/Tcf transcriptional complex [158].”
BackgroundDynamics of telomerase activity in response to acute psychological stress
Epel, E. S., Lin, J., Dhabhar, F. S., Wolkowitz, O. M., Puterman, E. M., Karan, L. D., & Blackburn, E. H. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.11.018 · Cited by 218 · see citing works
“Basic research on telomerase has shown it also has other roles in determining cellular programs and properties besides elongating telomeres (Hsu et al., 2007; Park et al., 2009).”
BackgroundGenomic Medicine and Implications for Hepatocellular Carcinoma Prevention and Therapy
Dhanasekaran, R., Nault, J., Roberts, L. R., & Zucman‐Rossi, J. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.11.001 · Cited by 208 · see citing works
Mitochondrial Telomerase Protects Cancer Cells from Nuclear DNA Damage and Apoptosis
Singhapol, C., Pal, D., Czapiewski, R., Porika, M., Nelson, G., & Saretzki, G. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0052989 · Cited by 195 · see citing works
“In recent years, however, evidence has accumulated that telomerase, and in particular its catalytic subunit TERT, is involved in various non-telomere-related functions such as regulation of gene expression, growth factors and cell proliferation [1–6].”
Assessing cell and organ senescence biomarkers
de Jesus, B. B., & Blasco, M. A. (2012) · Circulation Research · doi:10.1161/circresaha.111.247866 · Cited by 187 · see citing works
PAF and EZH2 Induce Wnt/β-Catenin Signaling Hyperactivation
Jung, H., Jun, S., Lee, M., Kim, H.-C., Wang, X., Ji, H. L., McCrea, P. D., & Park, J. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.08.028 · Cited by 185 · see citing works
Self-citationRole of progerin-induced telomere dysfunction in HGPS premature cellular senescence
Benson, E. K., Lee, S. W., & Aaronson, S. A. (2010) · Journal of Cell Science · doi:10.1242/jcs.067306 · Cited by 185 · see citing works
“For example, both wild-type and catalytically inactive mutant TERT are recruited to the promoters of growthcontrolling genes and function indistinguishably to modulate gene expression and enhance cell proliferation (Park et al., 2009; Zhou et al., 2009).”
Zhang, Y., Toh, L.-L., Lau, P., & Wang, X. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.368282 · Cited by 181 · see citing works
“(51) showed that hTERT plays an essential role in the Wnt/ -catenin signaling pathway by serving as a cofactor in a -catenin transcriptional complex.”
BackgroundTelomerase gene mutations are associated with cirrhosis formation
Hartmann, D., Srivastava, U., Thaler, M., Kleinhans, K. N., N'Kontchou, G., Scheffold, A., Bauer, K., Kratzer, R. F., Kloos, N., Katz, S.-F., et al. (2011) · Hepatology · doi:10.1002/hep.24217 · Cited by 173 · see citing works
“Recent studies have revealed telomere length-independent effects of TERT in regulating the transcriptional function of the Wnt-signaling pathway and stem cell activity in mice.(32) It remains to be seen whether cirrhosis-associated TERT mutations show defects in these noncanonical TERT-pathways and whether TERT mutati…”
BackgroundNoncanonical Functions of Telomerase: Implications in Telomerase-Targeted Cancer Therapies
Li, Y., & Tergaonkar, V. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-3568 · Cited by 171 · see citing works
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The Role of Telomere Biology in Cancer
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Role of shelterin in cancer and aging
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Healthy aging and disease: role for telomere biology?
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Telomerase regulates MYC-driven oncogenesis independent of its reverse transcriptase activity
Koh, C. M., Khattar, E., Leow, S. C., Liu, C. Y., Müller, J., Ang, W. X., Li, Y., Franzoso, G., Li, S., Guccione, E., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci79134 · Cited by 161 · see citing works
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Extra-telomeric Functions of Human Telomerase: Cancer, Mitochondria and Oxidative Stress
Saretzki, G. C. (2014) · Current Pharmaceutical Design · doi:10.2174/1381612820666140630095606 · Cited by 158 · see citing works
“In fact, they found that TERT can modulate the transcription of WNT target genes such as -catenin by acting as a transcriptional cofactor by interacting with the chromatin-remodelling factor BRG1 [66].”
BackgroundInfluentialGenetic studies provide clues on the pathogenesis of idiopathic pulmonary fibrosis
Kropski, J. A., Lawson, W. E., Young, L. R., & Blackwell, T. S. (2012) · Disease Models & Mechanisms · doi:10.1242/dmm.010736 · Cited by 154 · see citing works
HPV E6 protein interacts physically and functionally with the cellular telomerase complex
Liu, X., Dakic, A., Zhang, Y., Dai, Y., Chen, R., & Schlegel, R. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906357106 · Cited by 149 · see citing works
“It is very relevant that hTERT transcriptionally activates cellular gene sets that are very similar to those induced by the Wnt pathway (47) and might reflect its ability to convert primary keratinocytes into a stem-like state (mentioned above).”
Colon cancer therapy by focusing on colon cancer stem cells and their tumor microenvironment
Jahanafrooz, Z., Mosafer, J., Akbari, M., Hashemzaei, M., Mokhtarzadeh, A., & Baradaran, B. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.29337 · Cited by 148 · see citing works
“Higher level of β‐catenin in the nucleus also causes the expression of telomerase reverse transcriptase that identified as a characteristic of CCSC (Park et al., 2009).”
BackgroundWnt/β-catenin Signaling in Embryonic Stem Cell Self-renewal and Somatic Cell Reprogramming
Miki, T., Yasuda, S.-Y., & Kahn, M. (2011) · Stem Cell Reviews and Reports · doi:10.1007/s12015-011-9275-1 · Cited by 147 · see citing works
“Park et al reported that telomerase directly interacts with BRG1 and serves as a cofactor in a β-catenin transcriptional complex [87].”
BackgroundPovedano, J. M., Martinez, P., Serrano, R., Tejera, Á., Gómez-López, G., Bobadilla, M., Flores, J. M., Bosch, F., & Blasco, M. A. (2018) · eLife · doi:10.7554/elife.31299 · Cited by 139 · see citing works
Tejera, Á. M., d’Alcontres, M. S., Thanasoula, M., Marión, R. M., Martínez, P., Liao, C., Flores, J. M., Tarsounas, M., & Blasco, M. A. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.03.011 · Cited by 144 · see citing works
“…morphogenesis defects in Tpp1 null skin are not associated with a defective Wnt/β-catenin pathway, a known regulator of hair follicle development in mice ( Huelsken et al., 2001, Paus et al., 1999 and Zhang et al., 2008), recently described to be regulated by TERT levels (Park et al., 2009).”
BackgroundTelomere structure and telomerase in health and disease
Gomez, D. E., Armando, R. G., Fariña, H. G., Menna, P. L., Cerrudo, C. S., Ghiringhelli, P. D., & Alonso, D. F. (2012) · International Journal of Oncology · doi:10.3892/ijo.2012.1611 · Cited by 145 · see citing works
“Indeed, TERT can function as a transcriptional modulator of the Wnt-β-catenin signaling pathway (90).”
BackgroundJoseph, I., Tressler, R., Bassett, E., Harley, C. B., Buseman, C. M., Pattamatta, P., Wright, W. E., Shay, J. W., & Go, N. F. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-0233 · Cited by 144 · see citing works
CST Meets Shelterin to Keep Telomeres in Check
Giraud-Panis, M.-J. E., Teixeira, M. T., Géli, V., & Gilson, É. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.08.024 · Cited by 144 · see citing works
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Therapeutic Targeting of Telomerase
Jäger, K., & Walter, M. (2016) · Genes · doi:10.3390/genes7070039 · Cited by 142 · see citing works
“, as a cofactor in a β-catenin transcriptional complex [12], which plays a role in embryogenesis and development [13].”
BackgroundTelomere Length as Cardiovascular Aging Biomarker
De Meyer, T., Nawrot, T., Bekaert, S., De Buyzere, M. L., Rietzschel, E. R., & Andrés, V. (2018) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2018.06.014 · Cited by 139 · see citing works
Transcriptional outcome of telomere signalling
Ye, J., Renault, V. M., Jamet, K., & Gilson, É. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3743 · Cited by 140 · see citing works
Strong, M. A., Vidal-Cardenas, S. L., Karim, B. O., Yu, H. M., Guo, N., & Greider, C. W. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05312-11 · Cited by 134 · see citing works
“A previous publication (60) suggested that some mTERT / mice have missing ribs, which was interpreted as a Wnt pathway developmental defect.”
BackgroundInfluentialLiu, Y., Yang, M., Luo, J., & Zhou, H. (2020) · International Journal of Oral Science · doi:10.1038/s41368-020-00087-0 · Cited by 135 · see citing works
“In addition, the high expression of telomerase in CSCs helped maintain their self-renewal ability by playing a role in preventing DNA telomere shortening during cell division, thus allowing cells to proliferate indefinitely,(91) and promoting EMT of CSCs while still maintaining their stemness.(92,93) Therefore, the al…”
BackgroundHu, C.-J., Ni, Z., Li, B., Yong, X., Yang, X., Zhang, J.-W., Zhang, D., Qin, Y., Jie, M., Dong, H. F., et al. (2015) · Gut · doi:10.1136/gutjnl-2015-309322 · Cited by 131 · see citing works
Epigenetic regulation of aging stem cells
Pollina, E. A., & Brunet, A. (2011) · Oncogene · doi:10.1038/onc.2011.45 · Cited by 128 · see citing works
“Consistent with its prominent role in stem cell proliferation independent of its reverse transcriptase activity, TERT is a pivotal component of the transcriptional complex downstream of WNT signaling (Choi et al., 2008; Park et al., 2009).”
BackgroundDing, D., Peng, X., Zhou, J., Wang, M., & Cong, Y. (2013) · The FASEB Journal · doi:10.1096/fj.13-230904 · Cited by 129 · see citing works
“Recent findings suggest that telomerase acts as a transcriptional modulator of the Wnt- catenin signaling pathway and as an RNA-dependent RNA polymerase (10, 18).”
BackgroundShkreli, M., Sarin, K. Y., Pech, M. F., Papeta, N., Chang, W., Brockman, S. A., Cheung, P., Lee, E. Y., Kuhnert, F., Olson, J. L., et al. (2011) · Nature Medicine · doi:10.1038/nm.2550 · Cited by 127 · see citing works
“Based on our previous studies linking telomerase to the Wnt program 22–24 , we hypothesized that activation of Wnt signaling may underlie podocyte activation in i-TERT mice.”
Self-citationHrdličková, R., Nehyba, J., & Bose, H. R. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.00550-12 · Cited by 126 · see citing works
“The activation of the Wnt pathway has been correlated with the ability of the human TERT protein to stimulate cell proliferation (49).”
BackgroundInfluentialTelomeres and telomerase in prostate cancer development and therapy
Graham, M. K., & Meeker, A. K. (2017) · Nature Reviews Urology · doi:10.1038/nrurol.2017.104 · Cited by 122 · see citing works
Rheumatoid Arthritis: A Role for Immunosenescence?
Lindström, T. M., & Robinson, W. H. (2010) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2010.02965.x · Cited by 122 · see citing works
New prospects for targeting telomerase beyond the telomere
Arndt, G. M., & MacKenzie, K. L. (2016) · Nature reviews. Cancer · doi:10.1038/nrc.2016.55 · Cited by 120 · see citing works
LIG4 mediates Wnt signalling-induced radioresistance
Jun, S., Jung, Y., Suh, H. N., Wang, W., Kim, M. J., Oh, Y. S., Lien, E. M., Shen, X. H., Matsumoto, Y., McCrea, P. D., et al. (2016) · Nature Communications · doi:10.1038/ncomms10994 · Cited by 116 · see citing works
Self-citationRejuvenating the immune system in rheumatoid arthritis.
Weyand, C. M., Fujii, H., Shao, L., & Goronzy, J. J. (2009) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2009.180 · Cited by 112 · see citing works
The chromatin-remodeling enzyme BRG1 modulates vascular Wnt signaling at two levels
Griffin, C. T., Curtis, C. D., Davis, R. B., Muthukumar, V., & Magnuson, T. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013751108 · Cited by 111 · see citing works
“Previous studies have shown that BRG1 and β-catenin coregulateWnt signaling in nonvascular cells by mediating chromatin remodeling and transcriptional activation of Wnt target genes (32, 33).”
BackgroundLiu, N., Ding, D., Hao, W., Yang, F., Wu, X., Wang, M., Xu, X., Ju, Z., Liu, J., Song, Z., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw549 · Cited by 111 · see citing works
“It is therefore possible that hTERT recruits different proteins (Sp1, p65, Brg1 or -catenin) (34,40) and forms different protein complexes to regulate specific gene expression dependent on the target gene promoters and the cellular context.”
BackgroundTCFs and Wnt/β-catenin Signaling
Cadigan, K. M. (2012) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-386499-4.00001-x · Cited by 106 · see citing works
Maintenance of tumor initiating cells of defined genetic composition by nucleostemin
Okamoto, N., Yasukawa, M., Nguyen, C. L., Kasim, V., Maida, Y., Possemato, R., Shibata, T., Ligon, K. L., Fukami, K., Hahn, W. C., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015171108 · Cited by 106 · see citing works
“Recent work indicates that TERT regulates stem cell homeostasis independent of its function at telomeres (32) and that TERT, together with BRG1, modulates stem cell homeostasis by modulating the WNT/β-catenin signaling pathway (35).”
BackgroundTreating Cancer by Targeting Telomeres and Telomerase
Ivancich, M., Schrank, Z., Wojdyla, L. M., Leviskas, B., Kuckovic, A., Sanjali, A., & Puri, N. (2017) · Antioxidants · doi:10.3390/antiox6010015 · Cited by 106 · see citing works
Role of CDKN2A/p16 expression in the prognostication of oral squamous cell carcinoma
Padhi, S. S., Roy, S., Kar, M., Saha, A., Roy, S., Adhya, A. K., Baisakh, M. R., & Banerjee, B. (2017) · Oral Oncology · doi:10.1016/j.oraloncology.2017.07.030 · Cited by 108 · see citing works
HiChIRP reveals RNA-associated chromosome conformation
Mumbach, M. R., Granja, J. M., Flynn, R. A., Roake, C. M., Satpathy, A. T., Rubin, A. J., Qi, Y., Jiang, Z., Shams, S., Louie, B. H., et al. (2019) · Nature Methods · doi:10.1038/s41592-019-0407-x · Cited by 104 · see citing works
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Acetylsalicylic Acid Treatment Improves Differentiation and Immunomodulation of SHED
Liu, Y., Chen, C., Liu, S., Liu, D., Xu, X., Chen, X., & Shi, S. (2014) · Journal of Dental Research · doi:10.1177/0022034514557672 · Cited by 103 · see citing works
“Recently, evidence has suggested that TERT can regulate the Wnt/β-catenin pathway (Choi et al. 2008; Park et al. 2009).”
BackgroundTERT activation targets DNA methylation and multiple aging hallmarks
Shim, H. S., Iaconelli, J., Shang, X., Li, J., Lan, Z. D., Jiang, S., Nutsch, K., Beyer, B. A., Lairson, L. L., Boutin, A. T., et al. (2024) · Cell · doi:10.1016/j.cell.2024.05.048 · Cited by 104 · see citing works
Non-canonical Roles of Telomerase: Unraveling the Imbroglio
Ségal-Bendirdjian, E., & Géli, V. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00332 · Cited by 101 · see citing works
Separation of telomerase functions by reverse genetics
Mukherjee, S., Firpo, E. J., Wang, Y., & Roberts, J. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112414108 · Cited by 100 · see citing works
“Recent studies have shown that mTERT interacts with Brg-1, which binds β-catenin, and is thereby recruited to Wnt target genes, activating their transcription (16, 17).”
BackgroundInfluential
- 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
- Health Sciences › Medicine › Physiology › 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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