Replication of telomeres and the regulation of telomerase

Cold Spring Harbor Perspectives in Biology

Volumn 5, Issue 5, 2013, Pages

  Pfeiffer, Verena ^a   Lingner, Joachim ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

TELOMERASE;

ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; DNA REPLICATION; GENETICS; MAMMAL; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES; TELOMERE; TELOMERE HOMEOSTASIS;

ANIMALS; DNA REPLICATION; MAMMALS; MODELS, GENETIC; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS;

EID: 84877102552     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a010405     Document Type: Review

References (153)

1. Abreu E., Aritonovska E, Reichenbach P, Cristofari G, Culp B, Terns R.M., Lingner J, Terns MP. 2010. TIN2-tethered TPP1 recruits human telomerase to telomeres in vivo. Mol Cell Biol 30: 2971-2982.
2. Arneric M., Lingner J. 2007. Tel1 kinase and subtelomerebound Tbf1 mediate preferential elongation of short telomeres by telomerase in yeast. EMBO Rep 8: 1080-1085.
3. Arnoult N., Saintome C, Ourliac-Garnier I, Riou JF, Londono-Vallejo A. 2009. Human POT1 is required for efficient telomere C-rich strand replication in the absence of WRN. Genes Dev 23: 2915-2924.
4. Azzalin C.M., Reichenbach P, Khoriauli L, Giulotto E, Lingner J. 2007. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318: 798-801.
5. Bah A., Wischnewski H, Shchepachev V, Azzalin CM. 2012. The telomeric transcriptome of Schizosaccharomyces pombe. Nucleic Acids Res 40: 2995-3005.
6. Baumann P., Cech T. 2001. Pot1, the putative telomere endbinding protein in fission yeast and humans. Science 292: 1171-1175.
7. Beernink H.T., Miller K, Deshpande A, Bucher P, Cooper JP. 2003. Telomere maintenance in fission yeast requires an Est1 ortholog. Curr Biol 13: 575-580.
8. Bianchi A., Shore D. 2007a. Early replication of short telomeres in budding yeast. Cell 128: 1051-1062.
9. Bianchi A., Shore D. 2007b. Increased association of telomerase with short telomeres in yeast. Genes Dev 21: 1726-1730.
10. Bilaud T., Koering CE, Binet-Brasselet E, Ancelin K, Pollice A, Gasser S.M., Gilson E. 1996. The telobox, a Myb-related telomeric DNA binding motif found in proteins from yeast, plants and human. Nucleic Acids Res 24: 1294-1303.
11. Bilaud T., Brun C, Ancelin K, Koering CE, Laroche T, Gilson E. 1997. Telomeric localization of TRF2, a novel human telobox protein. Nat Genet 17: 236-239.
12. Blackburn EH. 2006. A history of telomere biology. In Telomeres, 2nd ed. (ed. de Lange T, Lundblad V, Blackburn EH), pp. 1-19. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
13. Blackburn E., Gall J. 1978. A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol 120: 33-53.
14. Bodnar A.G., Ouellette M, Frolkis M, Holt SE, Chiu C-P, Morin G.B., Harley CB, Shay JW, Lichtsteinter S, Wright WE. 1998. Extension of life-span by introduction of telomerase into normal human cells. Science 279: 349-352.
15. Bonetti D., Martina M, Clerici M, Lucchini G, Longhese MP. 2009. Multiple pathways regulate 3′ overhang generation at S. cerevisiae telomeres. Mol Cell 35: 70-81.
16. Broccoli D., Smogorzewska A, Chong L, de Lange T. 1997. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat Genet 17: 231-235.
17. Casteel D.E., Zhuang S, Zeng Y, Perrino FW, Boss GR, Goulian M., Pilz RB. 2009. A DNA polymerase-a. primase cofactor with homology to replication protein A-32 regulates DNA replication in mammalian cells. J Biol Chem 284: 5807-5818.
18. Chai W, Sfeir AJ, Hoshiyama H, Shay JW, Wright WE. 2006. The involvement of the Mre11/Rad50/Nbs1 complex in the generation of G-overhangs at human telomeres. EMBO Rep 7: 225-230.
19. Chang S., Multani AS, Cabrera NG, Naylor ML, Laud P, Lombard D., Pathak S, Guarente L, DePinho RA. 2004. Essential role of limiting telomeres in the pathogenesis of Werner syndrome. Nat Genet 36: 877-882.
20. Chang M., Arneric M, Lingner J. 2007. Telomerase repeat addition processivity is increased at critically short telomeres in a Tel1-dependent manner in Saccharomyces cerevisiae. Genes Dev 21: 2485-2494.
21. Chawla R., Redon S, Raftopoulou C, Wischnewski H, Gagos S, Azzalin CM. 2011. Human UPF1 interacts with TPP1 and telomerase and sustains telomere leadingstrand replication. EMBO J 30: 4047-4058.
22. Chen L.Y., Redon S, Lingner J. 2012. The human CST complex is a terminator of telomerase activity. Nature 488: 540-544.
23. Chong L., van Steensel B, Broccoli D, Erdjument-Bromage H, Hanish J., Tempst P, de Lange T. 1995. A human telomeric protein. Science 270: 1663-1667.
24. Cooper J.P., Nimmo ER, Allshire RC, Cech TR. 1997. Regulation of telomere length and function by aMyb-domain protein in fission yeast. Nature 385: 744-747.
25. Crabbe L., Verdun RE, Haggblom CI, Karlseder J. 2004. Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 306: 1951-1953.
26. Cristofari G., Adolf E, Reichenbach P, Sikora K, Terns RM, Terns M.P., Lingner J. 2007. Human telomerase RNA accumulation in Cajal bodies facilitates telomerase recruitment to telomeres and telomere elongation. Mol Cell 27: 882-889.
27. de Lange T. 2005. Shelterin: The protein complex that shapes and safeguards human telomeres. Genes Dev 19: 2100-2110.
28. de Lange T. 2009. How telomeres solve the end-protection problem. Science 326: 948-952.
29. Diede S.J., Gottschling DE. 2001. Exonuclease activity is required for sequence addition and Cdc13p loading at a de novo telomere. Curr Biol 11: 1336-1340.
30. Evans S.K., Lundblad V. 1999. Est1 and Cdc13 as comediators of telomerase access. Science 286: 117-120.
31. Ferreira H.C., Luke B, Schober H, Kalck V, Lingner J, Gasser SM. 2011. The PIAS homologue Siz2 regulates perinuclear telomere position and telomerase activity in budding yeast. Nat Cell Biol 13: 867-874.
32. Fisher T.S., Taggart AK, Zakian VA. 2004. Cell cycle-dependent regulation of yeast telomerase by Ku. Nat StructMol Biol 11: 1198-1205.
33. Flynn R.L., Centore RC, O'Sullivan RJ, Rai R, Tse A, Songyang Z, Chang S, Karlseder J, Zou L. 2011. TERRA and hnRNPA1 orchestrate an RPA-to-POT1 switch on telomeric single-stranded DNA. Nature 471: 532-536.
34. Forstemann K., Lingner J. 2001. Molecular basis for telomere repeat divergence in budding yeast. Mol Cell Biol 21: 7277-7286.
35. Frank C.J., Hyde M, Greider CW. 2006. Regulation of telomere elongation by the cyclin-dependent kinase CDK1. Mol Cell 24: 423-432.
36. Gallardo F., Olivier C, Dandjinou AT, Wellinger RJ, Chartrand P. 2008. TLC1 RNA nucleo-cytoplasmic trafficking links telomerase biogenesis to its recruitment to telomeres. EMBO J 27: 748-757.
37. Gallardo F., Laterreur N, Cusanelli E, Ouenzar F, Querido E, Wellinger R.J., Chartrand P. 2011. Live cell imaging of telomerase RNA dynamics reveals cell cycle-dependent clustering of telomerase at elongating telomeres. Mol Cell 44: 819-827.
38. Gao H., Cervantes RB, Mandell EK, Otero JH, Lundblad V. 2007. RPA-like proteins mediate yeast telomere function. Nat Struct Mol Biol 14: 208-214.
39. Gao H., Toro TB, Paschini M, Braunstein-Ballew B, Cervantes RB, Lundblad V. 2010. Telomerase recruitment in Saccharomyces cerevisiae is not dependent on Tel1-mediated phosphorylation of Cdc13. Genetics 186: 1147-1159.
40. Gottschling D., Zakian V. 1986. Telomere proteins: Specific recognition and protection of the natural termini of Oxytricha macronuclear DNA. Cell 47: 195-205.
41. Gottschling D.E., Aparicio OM, Billington BL, Zakian VA. 1990. Position effect at S. cerevisiae telomeres: Reversible repression of Pol II transcription. Cell 63: 751-762.
42. Gray J.T., Celander DW, Price CM, Cech TR. 1991. Cloning and expression of genes for the Oxytricha telomere-binding protein: Specific subunit interactions in the telomeric complex. Cell 67: 807-814.
43. Greenwood J., Cooper JP. 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.
44. Greider CW, Blackburn EH. 1985. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43: 405-413.
45. Greider C.W., Blackburn EH. 1989. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337: 331-337.
46. Griffith J.D., Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H., de Lange T. 1999. Mammalian telomeres end in a large duplex loop. Cell 97: 503-514.
47. Grossi S., Puglisi A, Dmitriev PV, Lopes M, Shore D. 2004. Pol12, the B subunit of DNA polymerase a, functions in both telomere capping and length regulation. Genes Dev 18: 992-1006.
48. Gu P., Min JN, Wang Y, Huang C, Peng T, Chai W, Chang S. 2012. CTC1 deletion results in defective telomere replication, leading to catastrophic telomere loss and stem cell exhaustion. EMBO J 31: 2309-2321.
49. Hang L.E., Liu X, Cheung I, Yang Y, Zhao X. 2011. SUMOylation regulates telomere length homeostasis by targeting Cdc13. Nat Struct Mol Biol 18: 920-926.
50. Hector R.E., Shtofman RL, Ray A, Chen BR, Nyun T, Berkner K.L., Runge KW. 2007. Tel1p preferentially associates with short telomeres to stimulate their elongation. Mol Cell 27: 851-858.
51. Hemann M.T., Strong MA, Hao LY, Greider CW. 2001. The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107: 67-77.
52. Hicke B.J., Celander DW, MacDonald GH, Price CM, Cech TR. 1990. Two versions of the gene encoding the 41-kilodalton subunit of the telomere binding protein of Oxytricha nova. Proc Natl Acad Sci 87: 1481-1485.
53. Hirano Y., Fukunaga K, Sugimoto K. 2009. Rif1 and Rif2 inhibit localization of Tel1 to DNA ends. Mol Cell 33: 312-322.
54. Hockemeyer D, Daniels JP, Takai H, de Lange T. 2006. Recent expansion of the telomeric complex in rodents: Two distinct POT1 proteins protect mouse telomeres. Cell 126: 63-77.
55. Huertas P., Aguilera A. 2003. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol Cell 12: 711-721.
56. Hug N., Lingner J. 2006. Telomere length homeostasis. Chromosoma 115: 413-425.
57. Iglesias N., Redon S, Pfeiffer V, Dees M, Lingner J, Luke B. 2011. Subtelomeric repetitive elements determine TERRA regulation by Rap1/Rif and Rap1/Sir complexes in yeast. EMBO Rep 12: 587-593.
58. Isken O., Maquat LE. 2008. The multiple lives of NMD factors: Balancing roles in gene and genome regulation. Nat Rev Genet 9: 699-712.
59. Ivessa A.S., Zhou JQ, Schulz VP, Monson EK, Zakian VA. 2002. Saccharomyces Rrm3p, a 5′ to 3′ DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev 16: 1383-1396.
60. Jady B.E., Bertrand E, Kiss T. 2004. Human telomerase RNA and box H/ACA scaRNAs share a common Cajal body-specific localization signal. J Cell Biol 164: 647-652.
61. Jady B.E., Richard P, Bertrand E, Kiss T. 2006. Cell cycledependent recruitment of telomerase RNA and Cajal bodies to human telomeres. Mol Biol Cell 17: 944-954.
62. Jain D., Cooper JP. 2010. Telomeric strategies: Means to an end. Annu Rev Genet 44: 243-269.
63. Kanoh J., Sadaie M, Urano T, Ishikawa F. 2005. Telomere binding protein Taz1 establishes Swi6 heterochromatin independently of RNAi at telomeres. Curr Biol 15: 1808-1819.
64. Kelleher C., Kurth I, Lingner J. 2005. Human protection of telomeres 1 (POT1) is a negative regulator of telomerase activity in vitro. Mol Cell Biol 25: 808-818.
65. Kim N.W., Piatyszek MA, Prowse KR, Harley CB, West MD, Ho P.L., Coviello GM, Wright WE, Weinrich SL, Shay JW. 1994. Specific association of human telomerase activity with immortal cells and cancer. Science 266: 2011-2015.
66. Koering C.E., Fourel G, Binet-Brasselet E, Laroche T, Klein F, Gilson E. 2000. Identification of high affinity Tbf1pbinding sites within the budding yeast genome. Nucleic Acids Res 28: 2519-2526.
67. Lam Y.C., Akhter S, Gu P, Ye J, Poulet A, Giraud-Panis MJ, Bailey S.M., Gilson E, Legerski RJ, Chang S. 2010. SNMIB/ Apollo protects leading-strand telomeres against NHEJmediated repair. EMBO J 29: 2230-2241.
68. Lansdorp PM. 2009. Telomeres and disease. EMBO J 28: 2532-2540.
69. Larrivee M., LeBel C, Wellinger RJ. 2004. The generation of proper constitutive G-tails on yeast telomeres is dependent on the MRX complex. Genes Dev 18: 1391-1396.
70. Latrick C.M., Cech TR. 2010. POT1-TPP1 enhances telomerase processivity by slowing primer dissociation and aiding translocation. EMBO J 29: 924-933.
71. Lee J., Mandell EK, Tucey TM, Morris DK, Lundblad V. 2008. The Est3 protein associateswith yeast telomerase through an OB-fold domain. Nat Struct Mol Biol 15: 990-997.
72. Lei M., Zaug AJ, Podell ER, Cech TR. 2005. Switching human telomerase on and off with hPOT1 protein in vitro. J Biol Chem 280: 20449-20456.
73. Lenain C., Bauwens S, Amiard S, Brunori M, Giraud-Panis M.J., Gilson E. 2006. The Apollo 5′ exonuclease functions together with TRF2 to protect telomeres from DNA repair. Curr Biol 16: 1303-1310.
74. Lendvay T.S., Morris DK, Sah J, Balasubramanian B, Lundblad V. 1996. Senescence mutants of Saccharomyces cerevisiae with a defect in telomere replication identify three additional EST genes. Genetics 144: 1399-1412.
75. Leonardi J., Box JA, Bunch JT, Baumann P. 2008. TER1, the RNA subunit of fission yeast telomerase. Nat Struct Mol Biol 15: 26-33.
76. Lewis K.A., Wuttke DS. 2012. Telomerase and telomere-associated proteins: Structural insights into mechanism and evolution. Structure 20: 28-39.
77. Li S., Makovets S, Matsuguchi T, Blethrow JD, Shokat KM, Blackburn EH. 2009. Cdk1-dependent phosphorylation of Cdc13 coordinates telomere elongation during cellcycle progression. Cell 136: 50-61.
78. Lingner J., Cech TR. 1996. Purification of telomerase from Euplotes aediculatus: Requirement of a primer 3′ overhang. Proc Natl Acad Sci 93: 10712-10717.
79. Lingner J., Cooper JP, Cech TR. 1995. Telomerase and DNA end replication: No longer a lagging strand problem? Science 269: 1533-1534.
80. Lingner J., Hughes TR, Shevchenko A, Mann M, Lundblad V, Cech TR. 1997. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276: 561-567.
81. Louis E.J., Borts RH. 1995. A complete set of marked telomeres in Saccharomyces cerevisiae for physical mapping and cloning. Genetics 139: 125-136.
82. Luke B., Panza A, Redon S, Iglesias N, Li Z, Lingner J. 2008. The Rat1p 5′ to 3′ exonuclease degrades telomeric repeatcontaining RNA and promotes telomere elongation in Saccharomyces cerevisiae. Mol Cell 32: 465-477.
83. Lundblad V., Szostak JW. 1989. A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 57: 633-643.
84. Lustig A.J., Kurtz S, Shore D. 1990. Involvement of the silencer and UAS binding protein RAP1 in regulation of telomere length. Science 250: 549-553.
85. Makovets S., Herskowitz I, Blackburn EH. 2004. Anatomy and dynamics ofDNA replication forkmovement in yeast telomeric regions. Mol Cell Biol 24: 4019-4031.
86. Marcand S., Gilson E, Shore D. 1997. A protein-counting mechanism for telomere length regulation in yeast. Science 275: 986-990.
87. Marcand S., Brevet V, Gilson E. 1999. Progressive cis-inhibition of telomerase upon telomere elongation. EMBOJ 18: 3509-3519.
88. Marcand S., Pardo B, Gratias A, Cahun S, Callebaut I. 2008. Multiple pathways inhibit NHEJ at telomeres. Genes Dev 22: 1153-1158.
89. Martin V., Du LL, Rozenzhak S, Russell P. 2007. Protection of telomeres by a conserved Stn1-Ten1 complex. Proc Natl Acad Sci 104: 14038-14043.
90. Martinez J.L., Edstrom JE, Morcillo G, Diez JL. 2001. Telomeres in Chironomus thummi are characterized by different subfamilies of complex DNA repeats. Chromosoma 110: 221-227.
91. Martinez P., Thanasoula M, Munoz P, Liao C, Tejera A, McNees C, Flores JM, Fernandez-Capetillo O, Tarsounas M, Blasco MA. 2009. Increased telomere fragility and fusions resulting from TRF1 deficiency lead to degenerative pathologies and increased cancer in mice. Genes Dev 23: 2060-2075.
92. McClintock B. 1941. The stability of broken ends of chromosomes in Zea mays. Genetics 41: 234-282.
93. Miller K.M., Rog O, Cooper JP. 2006. Semi-conservativeDNA replication through telomeres requires Taz1. Nature 440: 824-828.
94. Mimitou E.P., Symington LS. 2009. DNA end resection: Many nucleases make light work. DNA Repair (Amst) 8: 983-995.
95. Mitchell J.R., Cheng J, Collins K. 1999. A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 3′ end. Mol Cell Biol 19: 567-576.
96. Miyake Y., Nakamura M, Nabetani A, Shimamura S, Tamura M, Yonehara S, Saito M, Ishikawa F. 2009. RPAlike mammalian Ctc1-Stn1-Ten1 complex binds to single-stranded DNA and protects telomeres independently of the Pot1 pathway. Mol Cell 36: 193-206.
97. Miyoshi T., Kanoh J, Saito M, Ishikawa F. 2008. Fission yeast Pot1-Tpp1 protects telomeres and regulates telomere length. Science 320: 1341-1344.
98. Moser B.A., Chang YT, Kosti J, Nakamura TM. 2011. Tel1ATM and Rad3ATR kinases promote Ccq1-Est1 interaction to maintain telomeres in fission yeast. Nat Struct Mol Biol 18: 1408-1413.
99. Muller HJ. 1938. The remaking of chromosomes. Collecting Net (Woods Hole) 13: 181-198.
100. Nakamura T.M., Cech TR. 1998. Reversing time-origin of telomerase. Cell 92: 587-590.
101. Olovnikov AM. 1971. Principle of marginotomy in template synthesis of polynucleotides [in Russian]. Dokl Akad Nauk SSSR 201: 1496-1499.
102. Ottaviani A., Gilson E, Magdinier F. 2008. Telomeric position effect: From the yeast paradigm to human pathologies? Biochimie 90: 93-107.
103. Paeschke K., Capra JA, Zakian VA. 2011. DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase. Cell 145: 678-691.
104. Pardue M.L., Debaryshe PG. 2011. Retrotransposons that maintain chromosome ends. Proc Natl Acad Sci 108: 20317-20324.
105. Parkinson G.N., Lee MP, Neidle S. 2002. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 417: 876-880.
106. Pennock E., Buckley K, Lundblad V. 2001. Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104: 387-396.
107. Peterson S., Stellwagen A, Diede S, Singer M, Haimberger Z, Johnson C., Tzoneva M, Gottschling D. 2001. The function of a stem-loop in telomerase RNA is linked to the DNA repair protein Ku. Nat Genet 27: 64-67.
108. Pfingsten J.S., Goodrich KJ, Taabazuing C, Ouenzar F, Chartrand P., Cech TR. 2012. Mutually exclusive binding of telomerase RNA and DNA by Ku alters telomerase recruitment model. Cell 148: 922-932.
109. Pogacic V., Dragon F, Filipowicz W. 2000. Human H/ACA small nucleolar RNPs and telomerase share evolutionarily conserved proteins NHP2 and NOP10. Mol Cell Biol 20: 9028-9040.
110. Porro A., Feuerhahn S, Reichenbach P, Lingner J. 2010. Molecular dissection of TERRA biogenesis unveils the presence of distinct and multiple regulatory pathways. Mol Cell Biol 30: 4808-4817.
111. Price C.M., Boltz KA, Chaiken MF, Stewart JA, Beilstein MA, Shippen DE. 2010. Evolution of CST function in telomere maintenance. Cell Cycle 9: 3157-3165.
112. Qi H., Zakian VA. 2000. The Saccharomyces telomere-binding protein Cdc13p interacts with both the catalytic subunit ofDNA polymerase a and the telomerase-associated Est1 protein. Genes Dev 14: 1777-1788.
113. Raices M., Verdun RE, Compton SA, Haggblom CI, Griffith JD, Dillin A, Karlseder J. 2008. C. elegans telomeres contain G-strand and C-strand overhangs that are bound by distinct proteins. Cell 132: 745-757.
114. Redon S., Reichenbach P, Lingner J. 2007. Protein RNA and protein protein interactions mediate association of human EST1A/SMG6 with telomerase. Nucleic Acids Res 35: 7011-7022.
115. Reichenbach P., Hoss M, Azzalin CM, Nabholz M, Bucher P, Lingner J. 2003. A human homolog of yeast Est1 associates with telomerase and uncaps chromosome ends when overexpressed. Curr Biol 13: 568-574.
116. Riethman H. 2008. Human telomere structure and biology. Annu Rev Genomics Hum Genet 9: 1-19.
117. Ritchie K.B., Mallory JC, Petes TD. 1999. Interactions of TLC1 (which encodes the RNA subunit of telomerase), TEL1, and MEC1 in regulating telomere length in the yeast Saccharomyces cerevisiae. Mol Cell Biol 19: 6065-6075.
118. Sabourin M., Tuzon CT, Zakian VA. 2007. Telomerase and Tel1p preferentially associate with short telomeres in S. cerevisiae. Mol Cell 27: 550-561.
119. Schoeftner S., Blasco MA. 2008. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 10: 228-236.
120. Seto A.G., Zaug AJ, Sobel SG, Wolin SL, Cech TR. 1999. Saccharomyces cerevisiae telomerase is an Sm small nuclear ribonucleoprotein particle. Nature 401: 177-180.
121. Sfeir A.J., Chai W, Shay JW, Wright WE. 2005. Telomere-end processing the terminal nucleotides of human chromosomes. Mol Cell 18: 131-138.
122. Sfeir A., Kosiyatrakul ST, Hockemeyer D, MacRae SL, Karlseder J, Schildkraut CL, de Lange T. 2009. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138: 90-103.
123. Smogorzewska A., de Lange T. 2004. Regulation of telomerase by telomeric proteins. Annu Rev Biochem 73: 177-208.
124. Snow B.E., Erdmann N, Cruickshank J, Goldman H, Gill RM, Robinson M.O., Harrington L. 2003. Functional conservation of the telomerase protein Est1p in humans. Curr Biol 13: 698-704.
125. Sugawara N. 1989. DNA sequences at the telomeres of the fission yeast S. pombe. PhD thesis, Harvard University, Cambridge, MA.
126. Surovtseva Y.V., Churikov D, Boltz KA, Song X, Lamb JC, Warrington R., Leehy K, Heacock M, Price CM, Shippen DE. 2009. Conserved telomere maintenance component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Mol Cell 36: 207-218.
127. Takai K.K., Kibe T, Donigian JR, Frescas D, de Lange T. 2011. Telomere protection by TPP1/POT1 requires tethering to TIN2. Mol Cell 44: 647-659.
128. Tang W., Kannan R, Blanchette M, Baumann P. 2012. Telomerase RNA biogenesis involves sequential binding by Sm and Lsm complexes. Nature 484: 260-264.
129. Teixeira M.T., Arneric M, Sperisen P, Lingner J. 2004. Telomere length homeostasis is achieved via a switch between telomerase-extendible and-nonextendible states. Cell 117: 323-335.
130. Tomita K., Cooper JP. 2008. Fission yeast Ccq1 is telomerase recruiter and local checkpoint controller. Genes Dev 22: 3461-3474.
131. Tomlinson R.L., Ziegler TD, Supakorndej T, Terns RM, Terns MP. 2006. Cell cycle-regulated trafficking of human telomerase to telomeres. Mol Biol Cell 17: 955-965.
132. Tomlinson R.L., Li J, Culp BR, Terns RM, Terns MP. 2010. A Cajal body-independent pathway for telomerase trafficking in mice. Exp Cell Res 316: 2797-2809.
133. Tseng S.F., Lin JJ, Teng SC. 2006. The telomerase-recruitment domain of the telomere binding protein Cdc13 is regulated by Mec1p/Tel1p-dependent phosphorylation. Nucleic Acids Res 34: 6327-6336.
134. Tsukamoto Y., Taggart AK, Zakian VA. 2001. The role of the Mre11-Rad50-Xrs2 complex in telomerase-mediated lengthening of Saccharomyces cerevisiae telomeres. Curr Biol 11: 1328-1335.
135. Tycowski K.T., Shu MD, Kukoyi A, Steitz JA. 2009. A conserved WD40 protein binds the Cajal body localization signal of scaRNP particles. Mol Cell 34: 47-57.
136. van Overbeek M, de Lange T. 2006. Apollo, an Artemisrelated nuclease, interacts with TRF2 and protects human telomeres in S phase. Curr Biol 16: 1295-1302.
137. Vannier J.B., Pavicic-Kaltenbrunner V, Petalcorin MI, Ding H, Boulton SJ. 2012. RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 149: 795-806.
138. Venteicher A.S., Abreu EB, Meng Z, McCann KE, Terns RM, Veenstra T.D., Terns MP, Artandi SE. 2009. A human telomerase holoenzyme protein required for Cajal body localization and telomere synthesis. Science 323: 644-648.
139. Vodenicharov M.D., Wellinger RJ. 2006. DNA degradation at unprotected telomeres in yeast is regulated by the CDK1 (Cdc28/Clb) cell-cycle kinase. Mol Cell 24: 127-137.
140. Wahba L., Amon JD, Koshland D, Vuica-Ross M. 2011. RNase H and multiple RNA biogenesis factors cooperate to prevent RNA:DNA hybrids from generating genome instability. Mol Cell 44: 978-988.
141. Wang F., Podell ER, Zaug AJ, Yang Y, Baciu P, Cech TR, Lei M. 2007. The POT1-TPP1 telomere complex is a telomerase processivity factor. Nature 445: 506-510.
142. Watson J. 1972. Origin of concatemeric T7 DNA. Nat New Biol 239: 197-201.
143. Webb C.J., Zakian VA. 2008. Identification and characterization of the Schizosaccharomyces pombe TER1 telomerase RNA. Nat Struct Mol Biol 15: 34-42.
144. Webb C.J., Zakian VA. 2012. Schizosaccharomyces pombe Ccq1 and TER1 bind the 14-3-3-like domain of Est1, which promotes and stabilizes telomerase-telomere association. Genes Dev 26: 82-91.
145. Wu L., Multani AS, He H, Cosme-Blanco W, Deng Y, Deng J.M., Bachilo O, Pathak S, Tahara H, Bailey SM, et al. 2006. Pot1 deficiency initiates DNA damage checkpoint activation and aberrant homologous recombination at telomeres. Cell 126: 49-62.
146. Wu P., van Overbeek M, Rooney S, de Lange T. 2010. Apollo contributes to G overhang maintenance and protects leading-end telomeres. Mol Cell 39: 606-617.
147. Xin H., Liu D, Wan M, Safari A, Kim H, Sun W, O'Connor MS, Songyang Z. 2007. TPP1 is a homologue of ciliate TEBP-b and interacts with POT1 to recruit telomerase. Nature 445: 559-562.
148. Yamazaki H., Tarumoto Y, Ishikawa F. 2012. Tel1(ATM) and Rad3(ATR) phosphorylate the telomere protein Ccq1 to recruit telomerase and elongate telomeres in fission yeast. Genes Dev 26: 241-246.
149. Ye J., Lenain C, Bauwens S, Rizzo A, Saint-Leger A, Poulet A, Benarroch D., Magdinier F, Morere J, Amiard S, et al. 2010. TRF2 and Apollo cooperate with topoisomerase 2a to protect human telomeres from replicative damage. Cell 142: 230-242.
150. Yu G.L., Bradley JD, Attardi LD, Blackburn EH. 1990. In vivo alteration of telomere sequences and senescence caused by mutated Tetrahymena telomerase RNAs. Nature 344: 126-132.
151. Zhao Y., Sfeir AJ, Zou Y, Buseman CM, Chow TT, Shay JW, Wright WE. 2009. Telomere extension occurs at most chromosome ends and is uncoupled from fill-in in human cancer cells. Cell 138: 463-475.
152. Zhao Y., Abreu E, Kim J, Stadler G, Eskiocak U, Terns MP, Terns R.M., Shay JW, Wright WE. 2011. Processive and distributive extension of human telomeres by telomerase under homeostatic and nonequilibrium conditions. Mol Cell 42: 297-307.
153. Zhu XD, Kuster B, Mann M, Petrini JH, Lange T. 2000. Cell--cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 andhumantelomeres. Nat Genet 25: 347-352.