One identity or more for telomeres?

Frontiers in Oncology

Volumn 3 MAR, Issue , 2013, Pages

  Giraud Panis, Marie Josèphe ^a   Pisano, Sabrina ^a   Benarroch Popivker, Delphine ^a   Pei, Bei ^a   Du, Marie Hélène Le ^b   Gilson, Eric ^a,c  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b CEA   (France)

^c CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

Author keywords

Capping complexes; DNA topology; Telomeres; Telomeric chromatin organization

Indexed keywords

CAPPING PROTEIN; NUCLEOPROTEIN; PROTEIN; RNA POLYMERASE II; UNCLASSIFIED DRUG;

CHROMOSOME; DNA BINDING; DNA DAMAGE CHECKPOINT; DNA DENATURATION; DNA RECOMBINATION; DNA REPLICATION; DNA SEQUENCE; DNA TRANSCRIPTION; HETEROCHROMATIN; HUMAN; NONHUMAN; NUCLEOSOME; PROTEIN DNA INTERACTION; PROTEIN PROCESSING; REVIEW; TELOMERE;

EID: 84879838103     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00048     Document Type: Review

References (194)

1. Abad, J. P., and Villasante, A. (1999). The 3' non-coding region of the Drosophila melanogaster HeT-A telomeric retrotransposon contains sequences with propensity to form G-quadruplex DNA. FEBS Lett. 453, 59-62.
2. Abdallah, P., Luciano, P., Runge, K. W., Lisby, M., Geli, V., Gilson, E., et al. (2009). A two-step model for senescence triggered by a single critically short telomere. Nat. Cell Biol. 11, 988-993.
3. Ahmad, K., and Henikoff, S. (2002). The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9, 1191-1200.
4. Ahmed, S., and Henderson, E. (1992). Formation of novel hairpin structures by telomeric C-strand oligonucleotides. Nucleic Acids Res. 20, 507-511.
5. Alexander, M. K., and Zakian, V. A. (2003). Rap1p telomere association is not required for mitotic stability of a C(3)TA(2) telomere in yeast. EMBO J. 22, 1688-1696.
6. Allshire, R. C., and Karpen, G. H. (2008). Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat. Rev. Genet. 9, 923-937.
7. Amiard, S., Doudeau, M., Pinte, S., Poulet, A., Lenain, C., Faivre-Moskalenko, C., et al. (2007). A topological mechanism for TRF2-enhanced strand invasion. Nat. Struct. Mol. Biol. 14, 147-154.
8. Andreyeva, E. N., Belyaeva, E. S., Semeshin, V. F., Pokholkova, G. V., and Zhimulev, I. F. (2005). Three distinct chromatin domains in telomere ends of polytene chromosomes in Drosophila melanogaster Tel mutants. J. Cell Sci. 118, 5465-5477.
9. Arnoult, N., Schluth-Bolard, C., Letessier, A., Drascovic, I., Bouarich-Bourimi, R., Campisi, J., et al. (2010). Replication timing of human telomeres is chromosome arm-specific, influenced by subtelomeric structures and connected to nuclear localization. PLoS Genet. 6:e1000920. doi:10.1371/journal.pgen.1000920
10. Arnoult, N., Van Beneden, A., and Decottignies, A. (2012). Telomere length regulates TERRA levels through increased trimethylation of telomeric H3K9 and HP1alpha. Nat. Struct. Mol. Biol. 19, 948-956.
11. Arora, R., Brun, C. M., and Azzalin, C. M. (2012). Transcription regulates telomere dynamics in human cancer cells. RNA 18, 684-693.
12. Ascenzi, R., and Gantt, J. S. (1999). Subnuclear distribution of the entire complement of linker histone variants in Arabidopsis thaliana. Chromosoma 108, 345-355.
13. Azzalin, C. M., Reichenbach, P., Khoriauli, L., Giulotto, E., and Lingner, J. (2007). Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318, 798-801.
14. Bah, A., Gilson, E., and Wellinger, R. J. (2011). Telomerase is required to protect chromosomes with vertebrate-type T2AG3 3' ends in Saccharomyces cerevisiae. J. Biol. Chem. 286, 27132-27138.
15. Bankhead, T., Kobryn, K., and Chaconas, G. (2006). Unexpected twist: harnessing the energy in positive supercoils to control telomere resolution. Mol. Microbiol. 62, 895-905.
16. Bao, K., and Cohen, S. N. (2004). Reverse transcriptase activity innate to DNA polymerase I and DNA topoisomerase I proteins of Streptomyces telomere complex. Proc. Natl. Acad. Sci. U.S.A. 101, 14361-14366.
17. Bedoyan, J. K., Lejnine, S., Makarov, V. L., and Langmore, J. P. (1996). Condensation of rat telomere-specific nucleosomal arrays containing unusually short DNA repeats and histone H1. J. Biol. Chem. 271, 18485-18493.
18. Benetti, R., Schoeftner, S., Munoz, P., and Blasco, M. A. (2008). Role of TRF2 in the assembly of telomeric chromatin. Cell Cycle 7, 3461-3468.
19. Berthiau, A. S., Yankulov, K., Bah, A., Revardel, E., Luciano, P., Wellinger, R. J., et al. (2006). Subtelomeric proteins negatively regulate telomere elongation in budding yeast. EMBO J. 25, 846-856.
20. Bertuch, A. A., and Lundblad, V. (2006). The maintenance and masking of chromosome termini. Curr. Opin. Cell Biol. 18, 247-253.
21. Biffi, G., Tannahill, D., and Balasubramanian, S. (2012). An Intramolecular G-quadruplex structure is required for binding of telomeric repeat-containing RNA to the telomeric protein TRF2. J. Am. Chem. Soc. 134, 11974-11976.
22. Bilaud, T., Brun, C., Ancelin, K., Koering, C. E., Laroche, T., and Gilson, E. (1997). Telomeric localization of TRF2, a novel human telobox protein. Nat. Genet. 17, 236-239.
23. Bilaud, T., Koering, C. E., Binet-Brasselet, E., Ancelin, K., Pollice, A., Gasser, S. M., et al. (1996). The telobox, a Myb-related telomeric DNA binding motif found in proteins from yeast, plants and human. Nucleic Acids Res. 24, 1294-1303.
24. Biroccio, A., Porru, M., Rizzo, A., Salvati, E., D'Angelo, C., Orlandi, A., et al. (2011). DNA damage persistence as determinant of tumor sensitivity to the combination of Topo I inhibitors and telomere-targeting agents. Clin. Cancer Res. 17, 2227-2236.
25. Brevet, V., Berthiau, A. S., Civitelli, L., Donini, P., Schramke, V., Geli, V., et al. (2003). The number of vertebrate repeats can be regulated at yeast telomeres by Rap1-independent mechanisms. EMBO J. 22, 1697-1706.
26. Cacchione, S., Cerone, M. A., and Savino, M. (1997). In vitro low propensity to form nucleosomes of four telomeric sequences. FEBS Lett. 400, 37-41.
27. Canudas, S., Houghtaling, B. R., Bhanot, M., Sasa, G., Savage, S. A., Bertuch, A. A., et al. (2011). A role for heterochromatin protein 1gamma at human telomeres. Genes Dev. 25, 1807-1819.
28. Cesare, A. J., and Griffith, J. D. (2004). Telomeric DNA in ALT cells is characterized by free telomeric circles and heterogeneous t-loops. Mol. Cell. Biol. 24, 9948-9957.
29. Cesare, A. J., Groff-Vindman, C., Compton, S. A., McEachern, M. J., and Griffith, J. D. (2008). Telomere loops and homologous recombination-dependent telomeric circles in a Kluyveromyces lactis telomere mutant strain. Mol. Cell. Biol. 28, 20-29.
30. Cesare, A. J., Quinney, N., Willcox, S., Subramanian, D., and Griffith, J. D. (2003). Telomere looping in P. sativum (common garden pea). Plant J. 36, 271-279.
31. Chaconas, G., and Kobryn, K. (2010). Structure, function, and evolution of linear replicons in Borrelia. Annu. Rev. Microbiol. 64, 185-202.
32. Chikashige, Y., Haraguchi, T., and Hiraoka, Y. (2007). Another way to move chromosomes. Chromosoma 116, 497-505.
33. Chikashige, Y., Haraguchi, T., and Hiraoka, Y. (2010). Nuclear envelope attachment is not necessary for telomere function in fission yeast. Nucleus 1, 481-486.
34. Chuang, T. C., Moshir, S., Garini, Y., Chuang, A. Y., Young, I. T., Vermolen, B., et al. (2004). The three-dimensional organization of telomeres in the nucleus of mammalian cells. BMC Biol. 2:12. doi:10.1186/1741-7007-2-12
35. Cohen, P., and Blackburn, E. H. (1998). Two types of telomeric chromatin in Tetrahymena thermophila. J. Mol. Biol. 280, 327-344.
36. Court, R., Chapman, L., Fairall, L., and Rhodes, D. (2005). How the human telomeric proteins TRF1 and TRF2 recognize telomeric DNA: a view from high-resolution crystal structures. EMBO Rep. 6, 39-45.
37. Cowan, C. R., Carlton, P. M., and Cande, W. Z. (2001). The polar arrangement of telomeres in interphase and meiosis. Rabl organization and the bouquet. Plant Physiol. 125, 532-538.
38. Crabbe, L., Verdun, R. E., Haggblom, C. I., and Karlseder, J. (2004). Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 306, 1951-1953.
39. de Lange, T. (1992). Human telomeres are attached to the nuclear matrix. EMBO J. 11, 717-724.
40. De Vos, W. H., Hoebe, R. A., Joss, G. H., Haffmans, W., Baatout, S., Van Oostveldt, P., et al. (2009). Controlled light exposure microscopy reveals dynamic telomere microterritories throughout the cell cycle. Cytometry A 75, 428-439.
41. Dejardin, J., and Kingston, R. E. (2009). Purification of proteins associated with specific genomic Loci. Cell 136, 175-186.
42. Deng, Z., Campbell, A. E., and Lieberman, P. M. (2010). TERRA, CpG methylation and telomere heterochromatin: lessons from ICF syndrome cells. Cell Cycle 9, 69-74.
43. Deng, Z., Norseen, J., Wiedmer, A., Riethman, H., and Lieberman, P. M. (2009). TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol. Cell 35, 403-413.
44. Dimitrova, N., Chen, Y. C., Spector, D. L., and de Lange, T. (2008). 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456, 524-528.
45. Duquette, M. L., Handa, P., Vincent, J. A., Taylor, A. F., and Maizels, N. (2004). Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev. 18, 1618-1629.
46. Esmaili, N., and Leroy, J. L. (2005). i-Motif solution structure and dynamics of the d(AACCCC) and d(CCCCAA) tetrahymena telomeric repeats. Nucleic Acids Res. 33, 213-224.
47. Fairall, L., Chapman, L., Moss, H., de Lange, T., and Rhodes, D. (2001). Structure of the TRFH dimerization domain of the human telomeric proteins TRF1 and TRF2. Mol. Cell 8, 351-361.
48. Fanti, L., Giovinazzo, G., Berloco, M., and Pimpinelli, S. (1998). The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol. Cell 2, 527-538.
49. Farnung, B. O., Brun, C. M., Arora, R., Lorenzi, L. E., and Azzalin, C. M. (2012). Telomerase efficiently elongates highly transcribing telomeres in human cancer cells. PLoS ONE 7:e35714. doi: 10.1371/journal.pone.0035714
50. Ferreira, H. C., Luke, B., Schober, H., Kalck, V., Lingner, J., and Gasser, S. M. (2011). The PIAS homologue Siz2 regulates perinuclear telomere position and telomerase activity in budding yeast. Nat. Cell Biol. 13, 867-874.
51. Figueiredo, L. M., Pirrit, L. A., and Scherf, A. (2000). Genomic organisation and chromatin structure of Plasmodium falciparum chromosome ends. Mol. Biochem. Parasitol. 106, 169-174.
52. Filesi, I., Cacchione, S., De Santis, P., Rossetti, L., and Savino, M. (2000). The main role of the sequence-dependent DNA elasticity in determining the free energy of nucleosome formation on telomeric DNAs. Biophys. Chem. 83, 223-237.
53. Flynn, R. L., and Zou, L. (2010). Oligonucleotide/oligosaccharide-binding fold proteins: a growing family of genome guardians. Crit. Rev. Biochem. Mol. Biol. 45, 266-275.
54. Fourel, G., Revardel, E., Koering, C. E., and Gilson, E. (1999). Cohabitation of insulators and silencing elements in yeast subtelomeric regions. EMBO J. 18, 2522-2537.
55. Freitas-Junior, L. H., Porto, R. M., Pirrit, L. A., Schenkman, S., and Scherf, A. (1999). Identification of the telomere in Trypanosoma cruzi reveals highly heterogeneous telomere lengths in different parasite strains. Nucleic Acids Res. 27, 2451-2456.
56. Galati, A., Magdinier, F., Colasanti, V., Bauwens, S., Pinte, S., Ricordy, R., et al. (2012). TRF2 controls telomeric nucleosome organization in a cell cycle phase-dependent manner. PLoS ONE 7:e34386. doi:10.1371/journal.pone.0034386
57. Galati, A., Rossetti, L., Pisano, S., Chapman, L., Rhodes, D., Savino, M., et al. (2006). The human telomeric protein TRF1 specifically recognizes nucleosomal binding sites and alters nucleosome structure. J. Mol. Biol. 360, 377-385.
58. Garcia-Cao, M., O'Sullivan, R., Peters, A. H., Jenuwein, T., and Blasco, M. A. (2004). Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat. Genet. 36, 94-99.
59. Germe, T., Miller, K., and Cooper, J. P. (2009). A non-canonical function of topoisomerase II in disentangling dysfunctional telomeres. EMBO J. 28, 2803-2811.
60. Giraud-Panis, M. J., Pisano, S., Poulet, A., Le Du, M. H., and Gilson, E. (2010a). Structural identity of telomeric complexes. FEBS Lett. 584, 3785-3799.
61. Giraud-Panis, M. J., Teixeira, M. T., Geli, V., and Gilson, E. (2010b). CST meets shelterin to keep telomeres in check. Mol. Cell 39, 665-676.
62. Goldberg, A. D., Banaszynski, L. A., Noh, K. M., Lewis, P. W., Elsaesser, S. J., Stadler, S., et al. (2010). Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678-691.
63. Gonzalez-Suarez, I., and Gonzalo, S. (2010). Nurturing the genome: A-type lamins preserve genomic stability. Nucleus 1, 129-135.
64. Gottschling, D. E., and Cech, T. R. (1984). Chromatin structure of the molecular ends of Oxytricha macronuclear DNA: phased nucleosomes and a telomeric complex. Cell 38, 501-510.
65. Gottschling, D. E., and Zakian, V. A. (1986). Telomere proteins: specific recognition and protection of the natural termini of Oxytricha macronuclear DNA. Cell 47, 195-205.
66. Greenwood, J., and Cooper, J. P. (2012). Non-coding telomeric and subtelomeric transcripts are differentially regulated by telomeric and heterochromatin assembly factors in fission yeast. Nucleic Acids Res. 40, 2956-2963.
67. Griffith, J. D., Comeau, L., Rosenfield, S., Stansel, R. M., Bianchi, A., Moss, H., et al. (1999). Mammalian telomeres end in a large duplex loop. Cell 97, 503-514.
68. Hanaoka, S., Nagadoi, A., and Nishimura, Y. (2005). Comparison between TRF2 and TRF1 of their telomeric DNA-bound structures and DNA-binding activities. Protein Sci. 14, 119-130.
69. Hemann, M. T., and Greider, C. W. (1999). G-strand overhangs on telomeres in telomerase-deficient mouse cells. Nucleic Acids Res. 27, 3964-3969.
70. Henderson, E. R., and Blackburn, E. H. (1989). An overhanging 3' terminus is a conserved feature of telomeres. Mol. Cell. Biol. 9, 345-348.
71. Hinnebusch, J., and Barbour, A. G. (1991). Linear plasmids of Borrelia burgdorferi have a telomeric structure and sequence similar to those of a eukaryotic virus. J. Bacteriol. 173, 7233-7239.
72. Hiraoka, Y., and Dernburg, A. F. (2009). The SUN rises on meiotic chromosome dynamics. Dev. Cell 17, 598-605.
73. Horigome, C., Okada, T., Shimazu, K., Gasser, S. M., and Mizuta, K. (2011). Ribosome biogenesis factors bind a nuclear envelope SUN domain protein to cluster yeast telomeres. EMBO J. 30, 3799-3811.
74. Horvath, M. P., Schweiker, V. L., Bevilacqua, J. M., Ruggles, J. A., and Schultz, S. C. (1998). Crystal structure of the Oxytricha nova telomere end binding protein complexed with single strand DNA. Cell 95, 963-974.
75. Houghtaling, B. R., Canudas, S., and Smith, S. (2012). A role for sister telomere cohesion in telomere elongation by telomerase. Cell Cycle 11, 19-25.
76. Jacob, N. K., Kirk, K. E., and Price, C. M. (2003). Generation of telomeric G strand overhangs involves both G and C strand cleavage. Mol. Cell 11, 1021-1032.
77. Jain, D., Hebden, A. K., Nakamura, T. M., Miller, K. M., and Cooper, J. P. (2010). HAATI survivors replace canonical telomeres with blocks of generic heterochromatin. Nature 467, 223-227.
78. Jegou, T., Chung, I., Heuvelman, G., Wachsmuth, M., Gorisch, S. M., Greulich-Bode, K. M., et al. (2009). Dynamics of telomeres and promyelocytic leukemia nuclear bodies in a telomerase-negative human cell line. Mol. Biol. Cell 20, 2070-2082.
79. Kaminker, P. G., Kim, S. H., Desprez, P. Y., and Campisi, J. (2009). A novel form of the telomere-associated protein TIN2 localizes to the nuclear matrix. Cell Cycle 8, 931-939.
80. Karamysheva, Z. N., Surovtseva, Y. V., Vespa, L., Shakirov, E. V., and Shippen, D. E. (2004). A C-terminal Myb extension domain defines a novel family of double-strand telomeric DNA-binding proteins in Arabidopsis. J. Biol. Chem. 279, 47799-47807.
81. Kazda, A., Zellinger, B., Rossler, M., Derboven, E., Kusenda, B., and Riha, K. (2012). Chromosome end protection by blunt-ended telomeres. Genes Dev. 26, 1703-1713.
82. Khadaroo, B., Teixeira, M. T., Luciano, P., Eckert-Boulet, N., Germann, S. M., Simon, M. N., et al. (2009). The DNA damage response at eroded telomeres and tethering to the nuclear pore complex. Nat. Cell Biol. 11, 980-987.
83. Klapper, W., Qian, W., Schulte, C., and Parwaresch, R. (2003). DNA damage transiently increases TRF2 mRNA expression and telomerase activity. Leukemia 17, 2007-2015.
84. Ko, S., Jun, S. H., Bae, H., Byun, J. S., Han, W., Park, H., et al. (2008). Structure of the DNA-binding domain of NgTRF1 reveals unique features of plant telomere-binding proteins. Nucleic Acids Res. 36, 2739-2755.
85. Ko, S., Yu, E. Y., Shin, J., Yoo, H. H., Tanaka, T., Kim, W. T., et al. (2009). Solution structure of the DNA binding domain of rice telomere binding protein RTBP1. Biochemistry 48, 827-838.
86. Koering, C. E., Pollice, A., Zibella, M. P., Bauwens, S., Puisieux, A., Brunori, M., et al. (2002). Human telomeric position effect is determined by chromosomal context and telomeric chromatin integrity. EMBO Rep. 3, 1055-1061.
87. Konig, P., Giraldo, R., Chapman, L., and Rhodes, D. (1996). The crystal structure of the DNA-binding domain of yeast RAP1 in complex with telomeric DNA. Cell 85, 125-136.
88. Krafft, C., Benevides, J. M., and Thomas, G. J. Jr. (2002). Secondary structure polymorphism in Oxytricha nova telomeric DNA. Nucleic Acids Res. 30, 3981-3991.
89. Lam, Y. C., Akhter, S., Gu, P., Ye, J., Poulet, A., Giraud-Panis, M. J., et al. (2010). SNMIB/Apollo protects leading-strand telomeres against NHEJ-mediated repair. EMBO J. 29, 2230-2241.
90. Laporte, L., and Thomas, G. J. Jr. (1998). A hairpin conformation for the 3' overhang of Oxytricha nova telomeric DNA. J. Mol. Biol. 281, 261-270.
91. Lee, C. Y., Conrad, M. N., and Dresser, M. E. (2012). Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLoS Genet. 8:e1002730. doi:10.1371/journal.pgen.1002730
92. Lee, M. E., Rha, S. Y., Jeung, H. C., Kim, T. S., Chung, H. C., and Oh, B. K. (2008). Variation of the 3' telomeric overhang lengths in human cells. Cancer Lett. 264, 107-118.
93. Lejnine, S., Makarov, V. L., and Langmore, J. P. (1995). Conserved nucleoprotein structure at the ends of vertebrate and invertebrate chromosomes. Proc. Natl. Acad. Sci. U.S.A. 92, 2393-2397.
94. Leonetti, C., Scarsella, M., Riggio, G., Rizzo, A., Salvati, E., D'Incalci, M., et al. (2008). G-quadruplex ligand RHPS4 potentiates the antitumor activity of camptothecins in preclinical models of solid tumors. Clin. Cancer Res. 14, 7284-7291.
95. Lewis, K. A., and Wuttke, D. S. (2012). Telomerase and telomere-associated proteins: structural insights into mechanism and evolution. Structure 20, 28-39.
96. Lewis, L. K., Storici, F., Van Komen, S., Calero, S., Sung, P., and Resnick, M. A. (2004). Role of the nuclease activity of Saccharomyces cerevisiae Mre11 in repair of DNA double-strand breaks in mitotic cells. Genetics 166, 1701-1713.
97. Lewis, P. W., Elsaesser, S. J., Noh, K. M., Stadler, S. C., and Allis, C. D. (2010). Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl. Acad. Sci. U.S.A. 107, 14075-14080.
98. Li, B. (2010). A newly discovered role of telomeres in an ancient organism. Nucleus 1, 260-263.
99. Louis, S. F., Vermolen, B. J., Garini, Y., Young, I. T., Guffei, A., Lichtensztejn, Z., et al. (2005). c-Myc induces chromosomal rearrangements through telomere and chromosome remodeling in the interphase nucleus. Proc. Natl. Acad. Sci. U.S.A. 102, 9613-9618.
100. Lowell, J. E., and Cross, G. A. (2004). A variant histone H3 is enriched at telomeres in Trypanosoma brucei. J. Cell Sci. 117, 5937-5947.
101. Luderus, M. E., van Steensel, B., Chong, L., Sibon, O. C., Cremers, F. F., and de Lange, T. (1996). Structure, subnuclear distribution, and nuclear matrix association of the mammalian telomeric complex. J. Cell Biol. 135, 867-881.
102. Luke, B., Panza, A., Redon, S., Iglesias, N., Li, Z., and Lingner, J. (2008). The Rat1p 5' to 3' exonuclease degrades telomeric repeat-containing RNA and promotes telomere elongation in Saccharomyces cerevisiae. Mol. Cell 32, 465-477.
103. Madalena, C. R., Fernandes, T., Villasante, A., and Gorab, E. (2010). Curiously composite structures of a retrotransposon and a complex repeat associated with chromosome ends of Rhynchosciara americana (Diptera: Sciaridae). Chromosome Res. 18, 587-598.
104. Maillet, L., Boscheron, C., Gotta, M., Marcand, S., Gilson, E., and Gasser, S. M. (1996). Evidence for silencing compartments within the yeast nucleus: a role for telomere proximity and Sir protein concentration in silencer-mediated repression. Genes Dev. 10, 1796-1811.
105. Makarov, V. L., Hirose, Y., and Langmore, J. P. (1997). Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell 88, 657-666.
106. Malik, H. S., and Henikoff, S. (2003). Phylogenomics of the nucleosome. Nat. Struct. Biol. 10, 882-891.
107. Marcand, S., Brevet, V., Mann, C., and Gilson, E. (2000). Cell cycle restriction of telomere elongation. Curr. Biol. 10, 487-490.
108. Marian, C. O., Bordoli, S. J., Goltz, M., Santarella, R. A., Jackson, L. P., Danilevskaya, O., et al. (2003). The maize single myb histone 1 Gene, Smh1, belongs to a novel gene family and encodes a protein that binds telomere DNA repeats in vitro. Plant Physiol. 23, 23.
109. Mason, J. M., and Biessmann, H. (1995). The unusual telomeres of Drosophila. Trends Genet. 11, 58-62.
110. Mason, J. M., Frydrychova, R. C., and Biessmann, H. (2008). Drosophila telomeres: an exception providing new insights. Bioessays 30, 25-37.
111. Matot, B., Le Bihan, Y. V., Lescasse, R., Perez, J., Miron, S., David, G., et al. (2012). The orientation of the C-terminal domain of the Saccharomyces cerevisiae Rap1 protein is determined by its binding to DNA. Nucleic Acids Res. 40, 3197-3207.
112. McKittrick, E., Gafken, P. R., Ahmad, K., and Henikoff, S. (2004). Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl. Acad. Sci. U.S.A. 101, 1525-1530.
113. Miyoshi, T., Kanoh, J., Saito, M., and Ishikawa, F. (2008). Fission yeast Pot1-Tpp1 protects telomeres and regulates telomere length. Science 320, 1341-1344.
114. Molenaar, C., Wiesmeijer, K., Verwoerd, N. P., Khazen, S., Eils, R., Tanke, H. J., et al. (2003). Visualizing telomere dynamics in living mammalian cells using PNA probes. EMBO J. 22, 6631-6641.
115. Mondoux, M. A., Scaife, J. G., and Zakian, V. A. (2007). Differential nuclear localization does not determine the silencing status of Saccharomyces cerevisiae telomeres. Genetics 177, 2019-2029.
116. Moser, B. A., and Nakamura, T. M. (2009). Protection and replication of telomeres in fission yeast. Biochem. Cell Biol. 87, 747-758.
117. Munoz-Jordan, J. L., Cross, G. A., de Lange, T., and Griffith, J. D. (2001). T-loops at trypanosome telomeres. EMBO J. 20, 579-588.
118. Murzin, A. G. (1993). OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. EMBO J. 12, 861-867.
119. Nagai, S., Davoodi, N., and Gasser, S. M. (2011). Nuclear organization in genome stability: SUMO connections. Cell Res. 21, 474-485.
120. Nagai, S., Heun, P., and Gasser, S. M. (2010). Roles for nuclear organization in the maintenance of genome stability. Epigenomics 2, 289-305.
121. Nikitina, T., and Woodcock, C. L. (2004). Closed chromatin loops at the ends of chromosomes. J. Cell Biol. 166, 161-165.
122. O'Connor, M. S., Safari, A., Xin, H., Liu, D., and Songyang, Z. (2006). A critical role for TPP1 and TIN2 interaction in high-order telomeric complex assembly. Proc. Natl. Acad. Sci. U.S.A. 103, 11874-11879.
123. Oganesian, L., and Karlseder, J. (2011). Mammalian 5' C-rich telomeric overhangs are a mark of recombination-dependent telomere maintenance. Mol. Cell 42, 224-236.
124. Ottaviani, A., Gilson, E., and Magdinier, F. (2008). Telomeric position effect: from the yeast paradigm to human pathologies? Biochimie 90, 93-107.
125. Ottaviani, A., Schluth-Bolard, C., Rival-Gervier, S., Boussouar, A., Rondier, D., Foerster, A. M., et al. (2009). Identification of a perinuclear positioning element in human subtelomeres that requires A-type lamins and CTCF. EMBO J. 28, 2428-2436.
126. Oza, P., Jaspersen, S. L., Miele, A., Dekker, J., and Peterson, C. L. (2009). Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev. 23, 912-927.
127. Paeschke, K., Simonsson, T., Postberg, J., Rhodes, D., and Lipps, H. J. (2005). Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo. Nat. Struct. Mol. Biol. 12, 847-854.
128. Palladino, F., Laroche, T., Gilson, E., Axelrod, A., Pillus, L., and Gasser, S. M. (1993). SIR3 and SIR4 proteins are required for the positioning and integrity of yeast telomeres. Cell 75, 543-555.
129. Parseghian, M. H., Newcomb, R. L., and Hamkalo, B. A. (2001). Distribution of somatic H1 subtypes is non-random on active vs. inactive chromatin II: distribution in human adult fibroblasts. J. Cell. Biochem. 83, 643-659.
130. Pisano, S., Leoni, D., Galati, A., Rhodes, D., Savino, M., and Cacchione, S. (2010). The human telomeric protein hTRF1 induces telomere-specific nucleosome mobility. Nucleic Acids Res. 38, 2247-2255.
131. Pisano, S., Marchioni, E., Galati, A., Mechelli, R., Savino, M., and Cacchione, S. (2007). Telomeric nucleosomes are intrinsically mobile. J. Mol. Biol. 369, 1153-1162.
132. Pisano, S., Pascucci, E., Cacchione, S., De Santis, P., and Savino, M. (2006). AFM imaging and theoretical modeling studies of sequence-dependent nucleosome positioning. Biophys. Chem. 124, 81-89.
133. Porro, A., Feuerhahn, S., Reichenbach, P., and Lingner, J. (2010). Molecular dissection of telomeric repeat-containing RNA biogenesis unveils the presence of distinct and multiple regulatory pathways. Mol. Cell. Biol. 30, 4808-4817.
134. Poulet, A., Buisson, R., Faivre-Moskalenko, C., Koelblen, M., Amiard, S., Montel, F., et al. (2009). TRF2 promotes, remodels and protects telomeric Holliday junctions. EMBO J. 28, 641-651.
135. Poulet, A., Pisano, S., Faivre-Moskalenko, C., Pei, B., Tauran, Y., Haftek-Terreau, Z., et al. (2012). The N-terminal domains of TRF1 and TRF2 regulate their ability to condense telomeric DNA. Nucleic Acids Res. 40, 2566-2576.
136. Price, C. M., and Cech, T. R. (1987). Telomeric DNA-protein interactions of Oxytricha macronuclear DNA. Genes Dev. 1, 783-793.
137. Raffa, G. D., Ciapponi, L., Cenci, G., and Gatti, M. (2011). Terminin: a protein complex that mediates epigenetic maintenance of Drosophila telomeres. Nucleus 2, 383-391.
138. Raices, M., Verdun, R. E., Compton, S. A., Haggblom, C. I., Griffith, J. D., Dillin, A., et al. (2008). C. elegans telomeres contain G-strand and C-strand overhangs that are bound by distinct proteins. Cell 132, 745-757.
139. Ramirez, M. J., and Surralles, J. (2008). Laser confocal microscopy analysis of human interphase nuclei by three-dimensional FISH reveals dynamic perinucleolar clustering of telomeres. Cytogenet. Genome Res. 122, 237-242.
140. Ratnakumar, K., Duarte, L. F., LeRoy, G., Hasson, D., Smeets, D., Vardabasso, C., et al. (2012). ATRX-mediated chromatin association of histone variant macroH2A1 regulates alpha-globin expression. Genes Dev. 26, 433-438.
141. Roberts, N. Y., Osman, K., and Armstrong, S. J. (2009). Telomere distribution and dynamics in somatic and meiotic nuclei of Arabidopsis thaliana. Cytogenet. Genome Res. 124, 193-201.
142. Rong, Y. S. (2008). Loss of the histone variant H2A.Z restores capping to checkpoint-defective telomeres in Drosophila. Genetics 180, 1869-1875.
143. Rosenfeld, J. A., Wang, Z., Schones, D. E., Zhao, K., DeSalle, R., and Zhang, M. Q. (2009). Determination of enriched histone modifications in non-genic portions of the human genome. BMC Genomics 10:143. doi:10.1186/1471-2164-10-143
144. Rossetti, L., Cacchione, S., Fua, M., and Savino, M. (1998). Nucleosome assembly on telomeric sequences. Biochemistry 37, 6727-6737.
145. Routh, A., Sandin, S., and Rhodes, D. (2008). Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. Proc. Natl. Acad. Sci. U.S.A. 105, 8872-8877.
146. Rudenko, G., and Van der Ploeg, L. H. (1989). Transcription of telomere repeats in protozoa. EMBO J. 8, 2633-2638.
147. Salvati, E., Leonetti, C., Rizzo, A., Scarsella, M., Mottolese, M., Galati, R., et al. (2007). Telomere damage induced by the G-quadruplex ligand RHPS4 has an antitumor effect. J. Clin. Invest. 117, 3236-3247.
148. Salvati, E., Scarsella, M., Porru, M., Rizzo, A., Iachettini, S., Tentori, L., et al. (2010). PARP1 is activated at telomeres upon G4 stabilization: possible target for telomere-based therapy. Oncogene 29, 6280-6293.
149. Scherthan, H., Jerratsch, M., Li, B., Smith, S., Hulten, M., Lock, T., et al. (2000). Mammalian meiotic telomeres: protein composition and redistribution in relation to nuclear pores. Mol. Biol. Cell 11, 4189-4203.
150. Scherthan, H., Sfeir, A., and de Lange, T. (2011). Rap1-independent telomere attachment and bouquet formation in mammalian meiosis. Chromosoma 120, 151-157.
151. Schober, H., Ferreira, H., Kalck, V., Gehlen, L. R., and Gasser, S. M. (2009). Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev. 23, 928-938.
152. Schoeftner, S., and Blasco, M. A. (2008). Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat. Cell Biol. 10, 228-236.
153. Schoeftner, S., and Blasco, M. A. (2009). A 'higher order' of telomere regulation: telomere heterochromatin and telomeric RNAs. EMBO J. 28, 2323-2336.
154. Schrumpfova, P., Kuchar, M., Mikova, G., Skrisovska, L., Kubicarova, T., and Fajkus, J. (2004). Characterization of two Arabidopsis thaliana myb-like proteins showing affinity to telomeric DNA sequence. Genome 47, 316-324.
155. Sfeir, A., and de Lange, T. (2012). Removal of shelterin reveals the telomere end-protection problem. Science 336, 593-597.
156. Shareef, M. M., King, C., Damaj, M., Badagu, R., Huang, D. W., and Kellum, R. (2001). Drosophila heterochromatin protein 1 (HP1)/origin recognition complex (orc) protein is associated with HP1 and ORC and functions in heterochromatin-induced silencing. Mol. Biol. Cell 12, 1671-1685.
157. Siderakis, M., and Tarsounas, M. (2007). Telomere regulation and function during meiosis. Chromosome Res. 15, 667-679.
158. Solovei, I., Gaginskaya, E. R., and MacGregor, H. C. (1994). The arrangement and transcription of telomere DNA sequences at the ends of lampbrush chromosomes of birds. Chromosome Res. 2, 460-470.
159. Stansel, R. M., de Lange, T., and Griffith, J. D. (2001). T-loop assembly in vitro involves binding of TRF2 near the 3' telomeric overhang. EMBO J. 20, 5532-5540.
160. Sue, S. C., Hsiao, H. H., Chung, B. C., Cheng, Y. H., Hsueh, K. L., Chen, C. M., et al. (2006). Solution structure of the Arabidopsis thaliana telomeric repeat-binding protein DNA binding domain: a new fold with an additional C-terminal helix. J. Mol. Biol. 356, 72-85.
161. Sugiyama, T., Cam, H. P., Sugiyama, R., Noma, K., Zofall, M., Kobayashi, R., et al. (2007). SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 128, 491-504.
162. Surovtseva, Y. V., Churikov, D., Boltz, K. A., Song, X., Lamb, J. C., Warrington, R., et al. (2009). Conserved telomere maintenance component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Mol. Cell 36, 207-218.
163. Taddei, A., Schober, H., and Gasser, S. M. (2010). The budding yeast nucleus. Cold Spring Harb. Perspect. Biol. 2, a000612.
164. Therizols, P., Fairhead, C., Cabal, G. G., Genovesio, A., Olivo-Marin, J. C., Dujon, B., et al. (2006). Telomere tethering at the nuclear periphery is essential for efficient DNA double strand break repair in subtelomeric region. J. Cell Biol. 172, 189-199.
165. Tomaska, L., Makhov, A. M., Griffith, J. D., and Nosek, J. (2002). t-Loops in yeast mitochondria. Mitochondrion 1, 455-459.
166. Tomaska, L., Willcox, S., Slezakova, J., Nosek, J., and Griffith, J. D. (2004). Taz1 binding to a fission yeast model telomere: formation of telomeric loops and higher order structures. J. Biol. Chem. 279, 50764-50772.
167. Tomita, K., and Cooper, J. P. (2007). The telomere bouquet controls the meiotic spindle. Cell 130, 113-126.
168. Torigoe, H., and Furukawa, A. (2007). Tetraplex structure of fission yeast telomeric DNA and unfolding of the tetraplex on the interaction with telomeric DNA binding protein Pot1. J. Biochem. 141, 57-68.
169. Tsai, H. H., Huang, C. H., Tessmer, I., Erie, D. A., and Chen, C. W. (2011). Linear Streptomyces plasmids form superhelical circles through interactions between their terminal proteins. Nucleic Acids Res. 39, 2165-2174.
170. Tsai, J. H., and McKee, B. D. (2011). Homologous pairing and the role of pairing centers in meiosis. J. Cell Sci. 124, 1955-1963.
171. Vannier, J. B., Pavicic-Kaltenbrunner, V., Petalcorin, M. I., Ding, H., and Boulton, S. J. (2012). RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 149, 795-806.
172. Vaquero-Sedas, M. I., Gamez-Arjona, F. M., and Vega-Palas, M. A. (2011). Arabidopsis thaliana telomeres exhibit euchromatic features. Nucleic Acids Res. 39, 2007-2017.
173. Vaquero-Sedas, M. I., Luo, C., and Vega-Palas, M. A. (2012). Analysis of the epigenetic status of telomeres by using ChIP-seq data. Nucleic Acids Res. 40, e163.
174. Verdun, R. E., and Karlseder, J. (2006). The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 127, 709-720.
175. Vrbsky, J., Akimcheva, S., Watson, J. M., Turner, T. L., Daxinger, L., Vyskot, B., et al. (2010). siRNA-mediated methylation of Arabidopsis telomeres. PLoS Genet. 6:e1000986. doi:10.1371/journal.pgen.1000986
176. Wang, F., Podell, E. R., Zaug, A. J., Yang, Y., Baciu, P., Cech, T. R., et al. (2007). The POT1-TPP1 telomere complex is a telomerase processivity factor. Nature 445, 506-510.
177. Wang, R. C., Smogorzewska, A., and de Lange, T. (2004). Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119, 355-368.
178. Wang, X., Kam, Z., Carlton, P. M., Xu, L., Sedat, J. W., and Blackburn, E. H. (2008). Rapid telomere motions in live human cells analyzed by highly time-resolved microscopy. Epigenetics Chromatin 1, 4.
179. Watson, J. M., and Riha, K. (2010). Comparative biology of telomeres: where plants stand. FEBS Lett. 584, 3752-3759.
180. Weierich, C., Brero, A., Stein, S., von Hase, J., Cremer, C., Cremer, T., et al. (2003). Three-dimensional arrangements of centromeres and telomeres in nuclei of human and murine lymphocytes. Chromosome Res. 11, 485-502.
181. Wellinger, R. J., Wolf, A. J., and Zakian, V. A. (1993a). Origin activation and formation of single-strand TG1-3 tails occur sequentially in late S phase on a yeast linear plasmid. Mol. Cell. Biol. 13, 4057-4065.
182. Wellinger, R. J., Wolf, A. J., and Zakian, V. A. (1993b). Saccharomyces telomeres acquire single-strand TG1-3 tails late in S phase. Cell 72, 51-60.
183. Wong, L. H., Ren, H., Williams, E., McGhie, J., Ahn, S., Sim, M., et al. (2009). Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res. 19, 404-414.
184. Woodcock, C. L., Skoultchi, A. I., and Fan, Y. (2006). Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res. 14, 17-25.
185. Wright, J. H., Gottschling, D. E., and Zakian, V. A. (1992). Saccharomyces telomeres assume a non-nucleosomal chromatin structure. Genes Dev. 6, 197-210.
186. Wu, P., and de Lange, T. (2008). No overt nucleosome eviction at deprotected telomeres. Mol. Cell. Biol. 28, 5724-5735.
187. Wu, P., Takai, H., and de Lange, T. (2012). Telomeric 3' overhangs derive from resection by Exo1 and Apollo and fill-in by POT1b-associated CST. Cell 150, 39-52.
188. Ye, J., Lenain, C., Bauwens, S., Rizzo, A., Saint-Leger, A., Poulet, A., et al. (2010). TRF2 and Apollo cooperate with topoisomerase 2alpha to protect human telomeres from replicative damage. Cell 142, 230-242.
189. Ye, J. Z., Donigian, J. R., van Overbeek, M., Loayza, D., Luo, Y., Krutchinsky, A. N., et al. (2004). TIN2 binds TRF1 and TRF2 simultaneously and stabilizes the TRF2 complex on telomeres. J. Biol. Chem. 279, 47264-47271.
190. Yoshimura, S. H., Maruyama, H., Ishikawa, F., Ohki, R., and Takeyasu, K. (2004). Molecular mechanisms of DNA end-loop formation by TRF2. Genes Cells 9, 205-218.
191. Zaug, A. J., Podell, E. R., and Cech, T. R. (2005). Human POT1 disrupts telomeric G-quadruplexes allowing telomerase extension in vitro. Proc. Natl. Acad. Sci. U.S.A. 102, 10864-10869.
192. Zhang, L. F., Ogawa, Y., Ahn, J. Y., Namekawa, S. H., Silva, S. S., and Lee, J. T. (2009). Telomeric RNAs mark sex chromosomes in stem cells. Genetics 182, 685-698.
193. Zhang, Y. W., Zhang, Z. X., Miao, Z. H., and Ding, J. (2008). The telomeric protein TRF2 is critical for the protection of A549 cells from both telomere erosion and DNA double-strand breaks driven by salvicine. Mol. Pharmacol. 73, 824-832.
194. Zhou, Z., Du, X., Cai, Z., Song, X., Zhang, H., Mizuno, T., et al. (2012). Structure of Sad1-UNC84 homology (SUN) domain defines features of molecular bridge in nuclear envelope. J. Biol. Chem. 287, 5317-5326.