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A Protein-Counting Mechanism for Telomere Length Regulation in Yeast
Open accessAbstract
In the yeast Saccharomyces cerevisiae , telomere elongation is negatively regulated by the telomere repeat-binding protein Rap1p, such that a narrow length distribution of telomere repeat tracts is observed. This length regulation was shown to function independently of the orientation of the telomere repeats. The number of repeats at an individual telomere was reduced when hybrid proteins containing the Rap1p carboxyl terminus were targeted there by a heterologous DNA-binding domain. The extent of this telomere tract shortening was proportional to the number of targeted molecules, consistent with a feedback mechanism of telomere length regulation that can discriminate the precise number of Rap1p molecules bound to the chromosome end.
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“However, a strong common theme that has emerged is the likely involvement of a protein-counting mechanism in both systems (31, 44).”
From Control of Human Telomere Length by TRF1 and TRF2 (2000) · cites this paper as [31]
Citations
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Items 401–500 of 522
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“In the budding yeast Saccharomyces cerevisiae , Rap1, which binds telomeric double-stranded DNA repeats, inhibits both telomerase-dependent telomere elongation and telomere fusions by NHEJ [6-8].”
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“Emerging evidence suggests that, if the number of bound shelterin complexes (and hence the telomere length) is suYcient, TRF1 and TRF2 can repress telomerase activity at the chromosome end (Marcand et al. 1997).”
BackgroundA Sequence-Ready Map of the Human Chromosome 1q Telomere
Xiang, Z., Morse, E., Hu, X.-L., Jonathan Flint, C., Chi, H.-C., Grady, D. L., Moyzis, R. K., & Riethman, H. C. (2001) · Genomics · doi:10.1006/geno.2000.6448 · Cited by 7
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Natural diversity of telomere length distributions across 100 Saccharomyces cerevisiae strainsPreprint
Garrido, C., Gómez-Muñoz, C., Kornobis, É., Agier, N., Ilioaia, O., Fischer, G., & Xu, Z. (2026) · Genome Research · doi:10.1101/gr.281132.125 · Cited by 8
“In the budding yeast Saccharomyces cerevisiae , these include Rap1 and its cofactors Rif1/Rif2, which are bound to double-stranded DNA (dsDNA) in numbers roughly proportional to TL (Marcand et al. 1997; Levy and Black-burn 2004).”
Ng, Y. B., & Akıncılar, S. C. (2024) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2024.102460 · Cited by 7
Transcriptional profiling reveals the role of Candida albicans Rap1 in oxidative stress response
Wang, W., Chen, H., Chen, S.-Y., & Lan, C. (2024) · Bioscience Reports · doi:10.1042/bsr20240689 · Cited by 6
“In Saccharomyces cerevisiae , Rap1 plays an important role in subtelomeric gene silencing [15], telomere length control [16], and telomere end protection [17–19].”
Long telomeres: too much of a good thing
Chang, M. (2012) · BioMolecular Concepts · doi:10.1515/bmc-2012-0009 · Cited by 6
“Tethering Rap1, Rif1, or Rif2 to a telomere shortens the telomere in a manner that is proportional to the number of tethered molecules (38, 39) .”
BackgroundMultiple DNA Interactions Contribute to the Initiation of Telomerase Elongation
Andersson, A. K., Gustafsson, C., Krishnankutty, R., & Cohn, M. (2017) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.04.023 · Cited by 6
Yang, C., Nikolovska‐Coleska, Z., Li, P., Roller, P. P., & Wang, S. (2004) · The Journal of Physical Chemistry B · doi:10.1021/jp036009f · Cited by 6
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“Classic studies by Marcand et al. (1997) led to the proposal that telomere- length regulation is achieved through a ‘‘protein-counting’’ mechanism whereby higher numbers of proteins bound by a longer telomere repeat tract ultimately inhibit telomerase activity at that particular telomere (Figure 1).”
BackgroundMoriguchi, R., Ohata, K., Kanahama, K., Takahashi, H., Nishiyama, M., & Kanayama, Y. (2011) · Journal of Plant Physiology · doi:10.1016/j.jplph.2011.05.009 · Cited by 6
All Things Must End: Telomere Dynamics in YeastPreprint
DuBois, M. L., Diede, S. J., Stellwagen, A. E., & Gottschling, D. E. (2000) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2000.65.281 · Cited by 6
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“They are also more likely to be elongated by telomerase, which restores full protection 6,7 .”
Self-citationThe Bur1 cyclin‐dependent kinase regulates telomere length in Saccharomyces cerevisiae
Connelly, C. J., Vidal-Cardenas, S. L., Goldsmith, S., & Greider, C. W. (2021) · Yeast · doi:10.1002/yea.3680 · Cited by 4
“…Rad50/Xrs2 (MRX) complex mediate telomere elongation (Greenwell et al., 1995; Keener et al., 2019; Ritchie & Petes, 2000) and the Rap1/Rif1/Rif2 proteins and the Cdc13/Stn1/Ten1(CST) complex bind telomeres and regulate telomere length (Gao et al., 2007; Marcand et al., 1997; Price et al., 2010).”
BackgroundGallardo, F., Laterreur, N., Wellinger, R. J., & Chartrand, P. (2012) · RNA Biology · doi:10.4161/rna.21498 · Cited by 5
Elevated dosage of Ulp1 disrupts telomeric silencing in Saccharomyces cerevisiae
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Telomerase in Space and Time: Regulation of Yeast Telomerase Function at Telomeres and DNA Breaks
Vasianovich, Y., Krallis, A., & Wellinger, R. J. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.85750 · Cited by 5
Telomerase and non-Telomerase Mechanisms of Telomere Maintenance
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Functional Redundancy of the Duplex Telomeric DNA-binding Proteins in Arabidopsis
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Persistent Acetylation of Histone H3 Lysine 56 Compromises the Activity of DNA Replication Origins
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“41 Moreover we previously showed that cells with short telomeres are sensitive to NAM-induced sirtuin inhibition 27 ; we therefore considered the possibility that abnormal telomere elongation in rif1 D cells might favor NAM resistance.”
BackgroundCell-cycle-dependent telomere elongation by telomerase in budding yeast
Li, S. (2011) · Bioscience Reports · doi:10.1042/bsr20100095 · Cited by 4
Do cells sense time by number of divisions?
Schuss, Z., Tor, K., & Holcman, D. (2018) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2018.05.001 · Cited by 4
“Telomeres are necessary for the maintenance of chromosomal integrity and overall genomic stability [11, 21] and in the absence of (1)Tel-Aviv University, Tel-Aviv 69978, Israel.”
BackgroundLamb, J. C., Shakirov, E. V., & Shippen, D. E. (2011) · Springer eBooks · doi:10.1007/978-0-387-70869-0_7 · Cited by 4
The Rap1p-Telomere Complex Does Not Determine the Replicative Capacity of Telomerase-Deficient Yeast
Smolikov, S., & Krauskopf, A. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.23.8729-8739.2003 · Cited by 4
“It has been suggested that a telomere length-sensing system counts the number of telomeric repeats or proteins bound to them and translates this information to the machineries which add or deplete telomeric repeats (43, 55).”
BackgroundDynamics under the Telomeric Bridge
Pisano, S., Gilson, É., & Giraud-Panis, M.-J. E. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.11.005 · Cited by 4
“It also opens up the potential to explore the mechanisms protecting the 30 overhang from RPA binding (Takai et al., 2011) and to study the dynamics of assembly and disassembly of the bridge during the cell-cycle and telomerase regulation (Marcand et al., 1997).”
BackgroundCervoni, L., Ferraro, A., Eufemi, M., Fabio Altieri, F., Chichiarelli, S., & Turano, C. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.0115 · Cited by 4
Perspective/Review: Regulating telomere length from the inside out: The replication fork modelPreprint
Greider, C. W. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/041772 · Cited by 4
Determinants of chromosome-specific telomere lengths among 2573 All of Us participants
Jain, N., Luo, J., Yang, Y., Demanelis, K., Ahsan, H., Aschebrook‐Kilfoy, B., Chen, L. S., & Pierce, B. L. (2026) · Nature Communications · doi:10.1038/s41467-026-71172-x · Cited by 3
“The protein-counting model, a predominant model of TL regulation, proposes that telomeres are regulated around a similar mean distribution through preferential elongation of short telomeres and inhibitory effect of telomere-bound proteins on telomerase access to longer telomeres 59 .”
Feldmann, E. A., Koc, K. N., & Galletto, R. (2015) · Biophysical Chemistry · doi:10.1016/j.bpc.2015.01.002 · Cited by 3
“It has been proposed that Rap1 is a central component of a counting mechanism where the cell monitors and responds to the number of Rap1 molecules (or Rap1-Rif2) present at the telomere as a way of regulating access to telomerase (21, 22).”
BackgroundA comprehensive map of hotspots of de novo telomere addition in Saccharomyces cerevisiae
Ngo, K., Gittens, T. H., Gonzalez, D. I., Hatmaker, E. A., Plotkin, S., Engle, M., Friedman, G. A., Goldin, M., Hoerr, R. E., Eichman, B. F., et al. (2023) · Genetics · doi:10.1093/genetics/iyad076 · Cited by 2
Immortal transformation and telomerase reactivation of human mammary epithelial cells in culture
Stampfer, M. R., & Yaswen, P. (2001) · Advances in cell aging and gerontology · doi:10.1016/s1566-3124(01)08006-3 · Cited by 4
Telomere Structural Dynamics in Genome Integrity Control and Carcinogenesis
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Les télomères : du normal au pathologique
Marcand, S., Brun, B., Ancelin, K., & Gilson, É. (1997) · médecine/sciences · doi:10.4267/10608/543 · Cited by 3
Self-citationProtein Phosphatases and DNA Replication Initiation
Stark, M. J. R., Hiraga, S., & Donaldson, A. D. (2016) · Springer eBooks · doi:10.1007/978-3-319-24696-3_23 · Cited by 3
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Venditti, S., Stefano, G. D., & Mauro, E. D. (2000) · Molecular and General Genetics MGG · doi:10.1007/s004380000246 · Cited by 3
“…and Blackburn 1993); (2) processes based on telomere-length counting proteins (Fang and Cech 1995; McEachern and Blackburn 1995; Cooper et al. 1997; Marcand et al. 1997; Shore 1997; van Steensel and de Lange 1997); (3) Rap1-related (Huet et al. 1985; Shore and Nasmyth 1987; Fang and Cech 1995;…”
BackgroundSpontaneous replication fork collapse regulates telomere length homeostasis in wild-type yeast
Paschini, M., Gillespie, A. E., Reyes, C. M., McCoy, C. A., Lewis, K. A., Glustrom, L. W., Sharpee, T. O., Wuttke, D. S., & Lundblad, V. (2026) · Proceedings of the National Academy of Sciences · doi:10.1101/2020.08.05.237172 · Cited by 3
“The observation that there are two substrates for telomerase suggests a re-interpretation of the long-standing model that telomerase preferentially elongates short telomeres (26-30).”
Restriction on Ku’s Inward Translocation Caps Telomere EndsPreprint
Mattarocci, S., Baconnais, S., Roisné-Hamelin, F., Pobiega, S., Alibert, O., Morin, V., Deshayes, A., Veaute, X., Ropars, V., Chevreuil, M., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.22.629684 · Cited by 3
Self-citationThe adaptive molecular landscape of reprogrammed telomeric sequences
D’Angiolo, M., Barré, B. P., Khaiwal, S., Muenzner, J., Hallin, J., Chiara, M. D., Tellini, N., Warringer, J., Ralser, M., Gilson, É., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-71475-z · Cited by 2
“This enzyme is a reverse transcriptase that synthesizes new repeats using a RNA moiety as template (Chan & Blackburn, 2002; De Lange, 2005; Greider & Blackburn, 1989; Lundblad & Szostak, 1989; Marcand et al., 1997).”
Telomere length regulation by Rif1 protein from Hansenula polymorpha
Malyavko, A. N., Petrova, O. A., Zvereva, M. I., Polshakov, V. I., & Донцова, О. А. (2022) · eLife · doi:10.7554/elife.75010 · Cited by 2
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Yamazaki, H., Tarumoto, Y., & Ishikawa, F. (2012) · Genes & Development · doi:10.1101/gad.177873.111 · Cited by 74
“It has been suggested that budding yeast cells measure telomere length indirectly by counting the number of ds-telomere DNA-binding proteins (Rap1 in budding yeast) instead of directly measuring the telomere DNA length (protein-counting model) (Marcand et al. 1997).”
BackgroundTelomere configuration influences the choice of telomere maintenance pathways
Wen, W.-Y., Tsai, H.-J., Lin, C., Tseng, S., Wong, C., & Teng, S. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.03.011 · Cited by 2
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The leaves fall, yet the tree endures
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“In yeast, a “protein-counting” model posits that telomere shortening reduces available binding sites for telomere proteins acting as repressors (e.g., Rap1p), thereby permitting telomerase-mediated extension until a repressive threshold is restored [ 122].”
Gan, W., Pei, X., Yang, G., Zheng, G., Pan, Y., & Hu, P. (2026) · Cancer Treatment and Research Communications · doi:10.1016/j.ctarc.2026.101174 · Cited by 1
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Self-citationTelomeres and telomerase: revealing the end game
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Separating the effects of telomere size from the mechanism of telomere elongation
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BackgroundThe Relative Biologic Effectiveness versus Linear Energy Transfer Curve as a Cell Trait
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“Furthermore, a counting mechanism was proposed for telomere length regulation [21].”
BackgroundTelomeres and Chromosome Stability
Chu, T. W., & Autexier, C. (2016) · Springer eBooks · doi:10.1007/978-3-319-38882-3_6 · Cited by 1
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“A regulated competition between positive and negative factors creates a telomere homeostasis [12, 13] that in most eukaryotes acts as a dynamic telomere cap.”
BackgroundTelomere-Binding Proteins in Humans
Dimitrova, N. (2009) · Humana Press eBooks · doi:10.1007/978-1-60327-879-9_2 · Cited by 1
“Taken together, these experiments led to the conclusion that TRF1 plays a role in a ‘‘protein counting’’ mechanism, which presumes that the length of the telomeric array is translated into number of TRF1 molecules bound to telomere repeats (91, 94 ).”
BackgroundFrazer, L. N. (1998) · Mycological Research · doi:10.1017/s0953756297005443 · Cited by 1
Rif2 protects Rap1-depleted telomeres from MRX-mediated degradation in Saccharomyces cerevisiae
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“This model posits that Rap1, through its recruitment of Rif1 and Rif2, inhibits telomerase; the longer a telomere is, the more Rap1, Rif1, and Rif2 will be present, and the stronger the inhibition of telomerase will be (Marcand et al., 1997; Levy and Blackburn, 2004).”
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“In budding yeast, the telomere dsDNA-binding protein Rap1 serves to limit telomere length: the number of repeats at an individual telomere was reduced when hybrid proteins containing Rap1 were targeted there by a heterologous DNA-binding domain (Marcand et al., 1997).”
BackgroundFink, M. F. (2007) · Repository for Publications and Research Data (ETH Zurich) · doi:10.3929/ethz-a-005506702
“On the other hand, interaction of Rap1p with the Rif proteins negatively regulates telomere elongation (Kyrion et al., 1992; Marcand et al., 1999; Marcand et al., 1997; Wotton and Shore, 1997).”
BackgroundTelomere length homeostasis in the yeast "Saccharomyces cerevisiae"
Arnerić, M. (2007) · reroDoc Digital Library · doi:10.13097/archive-ouverte/unige:522
“Thus, the association, the “protein counting model” of telomere length control rather than the activity, of telomerase would be the regu(Marcand et al., 1997), in which telomerase-mediated lated element. telomere extension is regulated by the number of telo- To distinguish between these two models,…”
BackgroundInfluentialTelomere Structure in Telomerase Regulation
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Schleker, T. (2007) · edoc (University of Basel) · doi:10.5451/unibas-004360832
“This signal, which is Tel1-dependent, negatively regulates telomerase (Marcand et al., 1997).”
BackgroundTelomere dynamics and telomerase-independent cell survival in Arabidopsis thaliana
Watson, J. M. (2009) · OakTrust (Texas A&M University Libraries)
Telomere-associated proteins in Arabidopsis thaliana
Surovtseva, Y. V. (2008) · OakTrust (Texas A&M University Libraries)
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Cell cycle-dependent modification of Pot1 and its effects on telomere function
Kuznetsov, V. A. (2009) · OpenGrey (Institut de l'Information Scientifique et Technique)
Yeast telomeres: how to ignore essential double-strand DNA breaks?
Tomáška, Ľ., Sadovská, J., Nosek, J., & Griffith, J. D. (2003) · Journal of Applied Biomedicine · doi:10.32725/jab.2003.035
“The only known ortholog of a human telomeric protein – scRap1p, containing its own Myb domain – seems to fulfill functions divided between TRF proteins and hRap1p in mammalian cells (Marcand et al. 1997, McEachern et al. 2000).”
BackgroundThe Recognition and Mobility of DNA-Double Strand Breaks
Strecker, J. (2016) · TSpace (University of Toronto)
Telomere architecture and maintenance in schizosaccharomyces pombe
Pan, L. (2015) · KU ScholarWorks (The University of Kansas)
Structural studies on proteins involved in human telomere maintenance
Borucu, U. (2017) · DR-NTU (Nanyang Technological University) · doi:10.32657/10356/72778
Identification of the Telomerase RNA in the Filamentous Fungus Aspergillus oryzae
Davis, S. M. (2010) · Eukaryon
A dynamic control of human telomerase holoenzymePreprint
Sayed, M. E., Cheng, A., Yadav, G. P., Ludlow, A. T., Shay, J. W., Wright, W. E., & Jiang, Q. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/525733
A Theoretical Model of Telomere Length RegulationPreprint
Ishii, H. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/602037
“a ≡ kBT ln(k+/k0−), [11] b ≡ kBT ln β, [12] c ≡ kBT ln γ.”
The S. cerevisiae telomerase RNP: From assembly to action
Hass, E. P. (2017)
Mechanistic Model of Telomere Length Homeostasis in YeastPreprint
Singh, G., & Sriram, K. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.02.462846
Metadata
- Authors
- Marcand, S., Gilson, E., & Shore, D.
- Affiliations
- École Normale Supérieure de Lyon (FR)
- E. Gilson, Laboratoire de Biologie Moléculaire et Cellulaire, Ecole Normale Supérieure de Lyon, UMR49 CNRS/ENSL, 69364 Lyon Cédex 07, France.
- University of Geneva (CH)
- Corresponding author
- Marcand, Stéphane
- Shore, David
- Venue
- Science
- Published
- 1997-02-14
- Volume
- 275
- Issue
- 5302
- Pages
- 986-990
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W1978002329
- Cited by
- 524
- References
- 38
- Citations by year
- 2026: 10 · 2025: 4 · 2024: 7 · 2023: 6 · 2022: 5 · 2021: 14 · 2020: 5 · 2019: 17 · 2018: 10 · 2017: 12 · 2016: 13 · 2015: 9 · 2014: 14 · 2013: 14 · 2012: 10
- FWCI
- 23.60
- Type
- journal article
- Language
- en
- Open access
- Licence
- cc-by
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Funders
- National Institutes of Health (5r01gm040094-09)
- National Institute of General Medical Sciences (GM 40094)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- telomere length regulation, Rap1p, feedback regulation, protein-DNA interactions, telomere elongation, Saccharomyces cerevisiae, telomere shortening
- MeSH terms
- Binding Sites, Fungal Proteins, Genetic Markers, Mutation, Saccharomyces cerevisiae, Transformation, Genetic, Chromosomes, Fungal, Gene Expression Regulation, Fungal, Telomere, Telomerase, GTP-Binding Proteins, rap GTP-Binding Proteins
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