One Identity or More for Telomeres?

Giraud-Panis, Marie-Josèphe; Pisano, Sabrina; Benarroch-Popivker, Delphine; Pei, Bei; Du, Marie-Hélène Le; Gilson, Eric

doi:10.3389/fonc.2013.00048

Front. Oncol.

2013

DOI: 10.3389/fonc.2013.00048

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One Identity or More for Telomeres?

Marie-Josèphe Giraud-Panis

Sabrina Pisano

Delphine Benarroch-Popivker

et al.

Abstract: A major issue in telomere research is to understand how the integrity of chromosome ends is controlled. The fact that different types of nucleoprotein complexes have been described at the telomeres of different organisms raises the question of whether they have in common a structural identity that explains their role in chromosome protection. We will review here how telomeric nucleoprotein complexes are structured, comparing different organisms and trying to link these structures to telomere biology. It emerge… Show more

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Cited by 55 publications

(56 citation statements)

References 204 publications

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“…The length of telomeres and the chromatin organization of telomeric regions influence telomere functions. Hence, the epigenetic marks that label telomeric regions, which include telomeres and subtelomeres, play important roles in telomere biology (Blasco 2007;Galati et al 2013;Giraud-Panis et al 2013). …”

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Novel features of telomere biology revealed by the absence of telomeric DNA methylation

et al. 2016

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Cytosine methylation regulates the length and stability of telomeres, which can affect a wide variety of biological features, including cell differentiation, development, or illness. Although it is well established that subtelomeric regions are methylated, the presence of methylated cytosines at telomeres has remained controversial. Here, we have analyzed multiple bisulfite sequencing studies to address the methylation status of Arabidopsis thaliana telomeres. We found that the levels of estimated telomeric DNA methylation varied among studies. Interestingly, we estimated higher levels of telomeric DNA methylation in studies that produced C-rich telomeric strands with lower efficiency. However, these high methylation estimates arose due to experimental limitations of the bisulfite technique. We found a similar phenomenon for mitochondrial DNA: The levels of mitochondrial DNA methylation detected were higher in experiments with lower mitochondrial read production efficiencies. Based on experiments with high telomeric C-rich strand production efficiencies, we concluded that Arabidopsis telomeres are not methylated, which was confirmed by methylation-dependent restriction enzyme analyses. Thus, our studies indicate that telomeres are refractory to de novo DNA methylation by the RNA-directed DNA methylation machinery. This result, together with previously reported data, reveals that subtelomeric DNA methylation controls the homeostasis of telomere length.[Supplemental material is available for this article.]Telomeres guarantee the complete replication of chromosomal termini, prevent genome instability, and influence relevant systemic processes like aging, cancer, or illness (Blackburn 2010). The length of telomeres and the chromatin organization of telomeric regions influence telomere functions. Hence, the epigenetic marks that label telomeric regions, which include telomeres and subtelomeres, play important roles in telomere biology (Blasco 2007;Galati et al. 2013;Giraud-Panis et al. 2013).One of the major epigenetic signatures found in eukaryotes is cytosine methylation. This DNA modification regulates multiple processes in plants and animals, including the homeostasis of telomere length (Blasco 2007;Suzuki and Bird 2008;Ooi et al. 2009;Law and Jacobsen 2010;Castel and Martienssen 2013;Ogrocká et al. 2014;Vaquero-Sedas and Vega-Palas 2014). Mammalian DNA methylation is primarily found in the CG context (Ramsahoye et al. 2000;Lister et al. 2009). In contrast, plants have significant levels of DNA methylation in all sequence contexts (CG, CHG, and CHH, where H can be A, C, or T) (Law and Jacobsen 2010).Although subtelomeric DNA methylation has been reported in animals and plants, the presence of DNA methylation at telomeres remains an open question in both kingdoms (Blasco 2007;Vrbsky et al. 2010;Vaquero-Sedas et al. 2011;Ogrocká et al. 2014). The methylation status of mammalian telomeres has not been investigated because, as mentioned above, mammals have low levels of non-CG methylation, which is the type of DNA me...

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“…Since this early discovery, numerous variations in telomere nucleoprotein organization have been found [1]. For instance, in the budding yeast Saccharomyces cerevisiae, the 3′ overhang is bound by Cdc13, whereas the duplex portion is covered by an array of Rap1 proteins.…”

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“…The concept that telomere functionality relies on specific DNA-protein interactions stems from the discovery of the TEBPα/β heterodimer from Oxytrichia nova that binds to and protects the G-rich 3′ overhang that constitutes the end of telomeric DNA across many species [1]. Since this early discovery, numerous variations in telomere nucleoprotein organization have been found [1].…”

mentioning

confidence: 99%

“…The bridge is closed in S. pombe by Poz1, which contacts Rap1 and Tpz1, and in mammals by TIN2, which interacts simultaneously with TRF1, TRF2 and TPP1. Together with mammalian RAP1, which is recruited to telomeres via TRF2, and S. pombe Ccq1 bound to Tpz1, these bridged telomeric protein complexes have been named shelterin [1]. The shelterin is involved in most (if not all) telomeric functions: protection against activation of the DNA damage response (DDR), chromosome stability, telomerase regulation, long and short range transcriptional regulation and meiosis.…”

mentioning

confidence: 99%

“…It also suggests a common evolutionary origin for these domains despite their low level of sequence identity, which makes their identification by standard homology search algorithms difficult. Various plants and Trypanosoma, organisms that are distantly related to metazoans and fungi, express proteins that contain a telobox at their C-terminus [1] and an N-terminal domain that is likely to fold into a TRFH structure (although its structure has not been solved yet). If confirmed, this would suggest that analyzed the structure of the N-terminal part of human TIN2, which shows a similar architecture to that of S. pombe Poz1.…”

mentioning

confidence: 99%

See 2 more Smart Citations

TRFH domain: at the root of telomere protein evolution?

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Gilson

2017

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Self Cite

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One Identity or More for Telomeres?

Cited by 55 publications

References 204 publications

Novel features of telomere biology revealed by the absence of telomeric DNA methylation

TRFH domain: at the root of telomere protein evolution?

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