TIN2-Tethered TPP1 Recruits Human Telomerase to Telomeres In Vivo

REFERENCES

• Almeida, F., R. Saffrich, W. Ansorge, and M. Carmo-Fonseca. 1998. Microinjection of anti-coilin antibodies affects the structure of coiled bodies. J. Cell Biol. 142:899–912.
   PubMedGoogle Scholar
• Armanios, M. Y., J. J. Chen, J. D. Cogan, J. K. Alder, R. G. Ingersoll, C. Markin, W. E. Lawson, M. Xie, I. Vulto, J. A. Phillips III, P. M. Lansdorp, C. W. Greider, and J. E. Loyd. 2007. Telomerase mutations in families with idiopathic pulmonary fibrosis. N. Engl. J. Med. 356:1317–1326.
   PubMed Web of Science ®Google Scholar
• Autexier, C., R. Pruzan, W. D. Funk, and C. W. Greider. 1996. Reconstitution of human telomerase activity and identification of a minimal functional region of the human telomerase RNA. EMBO J. 15:5928–5935.
   PubMed Web of Science ®Google Scholar
• Azzalin, C. M., and J. Lingner. 2006. The human RNA surveillance factor UPF1 is required for S phase progression and genome stability. Curr. Biol. 16:433–439.
   PubMedGoogle Scholar
• Azzalin, C. M., P. Reichenbach, L. Khoriauli, E. Giulotto, and J. Lingner. 2007. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318:798–801.
   PubMed Web of Science ®Google Scholar
• Baumann, P., and T. Cech. 2001. Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292:1171–1175.
   PubMed Web of Science ®Google Scholar
• Bodnar, A. G., M. Ouellette, M. Frolkis, S. E. Holt, C.-P. Chiu, G. B. Morin, C. B. Harley, J. W. Shay, S. Lichtsteinter, and W. E. Wright. 1998. Extension of life-span by introduction of telomerase into normal human cells. Science 279:349–352.
   PubMed Web of Science ®Google Scholar
• Broccoli, D., A. Smogorzewska, L. Chong, and T. de Lange. 1997. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat. Genet. 17:231–235.
   PubMed Web of Science ®Google Scholar
• Chandra, A., T. R. Hughes, C. I. Nugent, and V. Lundblad. 2001. Cdc13 both positively and negatively regulates telomere replication. Genes Dev. 15:404–414.
   PubMedGoogle Scholar
• Cong, Y. S., W. E. Wright, and J. W. Shay. 2002. Human telomerase and its regulation. Microbiol. Mol. Biol. Rev. 66:407–425.
   PubMed Web of Science ®Google Scholar
• Crabbe, L., R. E. Verdun, C. I. Haggblom, and J. Karlseder. 2004. Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 306:1951–1953.
   PubMed Web of Science ®Google Scholar
• Cristofari, G., E. Adolf, P. Reichenbach, K. Sikora, R. M. Terns, M. P. Terns, and J. Lingner. 2007. Human telomerase RNA accumulation in Cajal bodies facilitates telomerase recruitment to telomeres and telomere elongation. Mol. Cell 27:882–889.
   PubMed Web of Science ®Google Scholar
• Cristofari, G., and J. Lingner. 2006. Telomere length homeostasis requires that telomerase levels are limiting. EMBO J. 25:565–574.
   PubMed Web of Science ®Google Scholar
• Cristofari, G., K. Sikora, and J. Lingner. 2007. Telomerase unplugged. ACS Chem. Biol. 2:155–158.
   PubMedGoogle Scholar
• d'Adda di Fagagna, F., P. M. Reaper, L. Clay-Farrace, H. Fiegler, P. Carr, T. Von Zglinicki, G. Saretzki, N. P. Carter, and S. P. Jackson. 2003. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426:194–198.
   PubMed Web of Science ®Google Scholar
• de Lange, T. 2005. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19:2100–2110.
   PubMed Web of Science ®Google Scholar
• Denchi, E. L., and T. de Lange. 2007. Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 448:1068–1071.
   PubMed Web of Science ®Google Scholar
• Greider, C. W., and E. H. Blackburn. 1989. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337:331–337.
   PubMed Web of Science ®Google Scholar
• Guo, X., Y. Deng, Y. Lin, W. Cosme-Blanco, S. Chan, H. He, G. Yuan, E. J. Brown, and S. Chang. 2007. Dysfunctional telomeres activate an ATM-ATR-dependent DNA damage response to suppress tumorigenesis. EMBO J. 26:4709–4719.
   PubMedGoogle Scholar
• Hockemeyer, D., W. Palm, T. Else, J. P. Daniels, K. K. Takai, J. Z. Ye, C. E. Keegan, T. de Lange, and G. D. Hammer. 2007. Telomere protection by mammalian Pot1 requires interaction with Tpp1. Nat. Struct. Mol. Biol. 14:754–761.
   PubMed Web of Science ®Google Scholar
• Hockemeyer, D., A. J. Sfeir, J. W. Shay, W. E. Wright, and T. de Lange. 2005. POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end. EMBO J. 24:2667–2678.
   PubMed Web of Science ®Google Scholar
• Jady, B. E., E. Bertrand, and T. Kiss. 2004. Human telomerase RNA and box H/ACA scaRNAs share a common Cajal body-specific localization signal. J. Cell Biol. 164:647–652.
   PubMed Web of Science ®Google Scholar
• Jady, B. E., P. Richard, E. Bertrand, and T. Kiss. 2006. Cell cycle-dependent recruitment of telomerase RNA and Cajal bodies to human telomeres. Mol. Biol. Cell 17:944–954.
   PubMed Web of Science ®Google Scholar
• Kibe, T., G. A. Osawa, C. E. Keegan, and T. de Lange. 2010. Telomere protection by TPP1 is mediated by POT1a and POT1b. Mol. Cell. Biol. 30:1059–1066.
   PubMed Web of Science ®Google Scholar
• Kim, S. H., C. Beausejour, A. R. Davalos, P. Kaminker, S. J. Heo, and J. Campisi. 2004. TIN2 mediates functions of TRF2 at human telomeres. J. Biol. Chem. 279:43799–43804.
   PubMed Web of Science ®Google Scholar
• Kondo, T., N. Oue, K. Yoshida, Y. Mitani, K. Naka, H. Nakayama, and W. Yasui. 2004. Expression of POT1 is associated with tumor stage and telomere length in gastric carcinoma. Cancer Res. 64:523–529.
   PubMedGoogle Scholar
• Lansdorp, P. M. 2009. Telomeres and disease. EMBO J. 28:2532–2540.
   PubMed Web of Science ®Google Scholar
• Latrick, C. M., and T. R. Cech. 2010. POT1-TPP1 enhances telomerase processivity by slowing primer dissociation and aiding translocation. EMBO J. 29:924–933.
   PubMed Web of Science ®Google Scholar
• Lei, M., E. R. Podell, and T. R. Cech. 2004. Structure of human POT1 bound to telomeric single-stranded DNA provides a model for chromosome end-protection. Nat. Struct. Mol. Biol. 11:1223–1229.
   PubMed Web of Science ®Google Scholar
• Li, S., S. Makovets, T. Matsuguchi, J. D. Blethrow, K. M. Shokat, and E. H. Blackburn. 2009. Cdk1-dependent phosphorylation of Cdc13 coordinates telomere elongation during cell-cycle progression. Cell 136:50–61.
   PubMed Web of Science ®Google Scholar
• Lin, J. J., and V. A. Zakian. 1996. The Saccharomyces CDC13 protein is a single-strand TG1-3 telomeric DNA-binding protein in vitro that affects telomere behavior in vivo. Proc. Natl. Acad. Sci. U. S. A. 93:13760–13765.
   PubMedGoogle Scholar
• Lingner, J., T. R. Hughes, A. Sherchenko, M. Mann, V. Lundblad, and T. R. Cech. 1997. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276:561–567.
   PubMed Web of Science ®Google Scholar
• Liu, D., A. Safari, M. S. O'Connor, D. W. Chan, A. Laegeler, J. Qin, and Z. Songyang. 2004. PTOP interacts with POT1 and regulates its localization to telomeres. Nat. Cell Biol. 6:673–680.
   PubMed Web of Science ®Google Scholar
• Loayza, D., and T. De Lange. 2003. POT1 as a terminal transducer of TRF1 telomere length control. Nature 424:1013–1018.
   PubMed Web of Science ®Google Scholar
• Nugent, C. I., T. R. Hughes, N. F. Lue, and V. Lundblad. 1996. Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274:249–252.
   PubMedGoogle Scholar
• Paeschke, K., S. Juranek, T. Simonsson, A. Hempel, D. Rhodes, and H. J. Lipps. 2008. Telomerase recruitment by the telomere end binding protein-beta facilitates G-quadruplex DNA unfolding in ciliates. Nat. Struct. Mol. Biol. 15:598–604.
   PubMed Web of Science ®Google Scholar
• Paeschke, K., T. Simonsson, J. Postberg, D. Rhodes, and H. J. Lipps. 2005. Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo. Nat. Struct. Mol. Biol. 12:847–854.
   PubMed Web of Science ®Google Scholar
• Palm, W., and T. de Lange. 2008. How shelterin protects mammalian telomeres. Annu. Rev. Genet. 42:301–334.
   PubMed Web of Science ®Google Scholar
• Savage, S. A., N. Giri, G. M. Baerlocher, N. Orr, P. M. Lansdorp, and B. P. Alter. 2008. TINF2, a component of the shelterin telomere protection complex, is mutated in dyskeratosis congenita. Am. J. Hum. Genet. 82:501–509.
   PubMed Web of Science ®Google Scholar
• Smogorzewska, A., and T. De Lange. 2004. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem. 73:177–208.
   PubMed Web of Science ®Google Scholar
• Smogorzewska, A., B. van Steensel, A. Bianchi, S. Oelmann, M. R. Schaefer, G. Schnapp, and T. de Lange. 2000. Control of human telomere length by TRF1 and TRF2. Mol. Cell. Biol. 20:1659–1668.
   PubMed Web of Science ®Google Scholar
• Takai, H., A. Smogorzewska, and T. de Lange. 2003. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13:1549–1556.
   PubMed Web of Science ®Google Scholar
• Tomlinson, R. L., E. B. Abreu, T. Ziegler, H. Ly, C. M. Counter, R. M. Terns, and M. P. Terns. 2008. Telomerase reverse transcriptase is required for the localization of telomerase RNA to cajal bodies and telomeres in human cancer cells. Mol. Biol. Cell 19:3793–3800.
   PubMedGoogle Scholar
• Tomlinson, R. L., T. D. Ziegler, T. Supakorndej, R. M. Terns, and M. P. Terns. 2006. Cell cycle-regulated trafficking of human telomerase to telomeres. Mol. Biol. Cell 17:955–965.
   PubMed Web of Science ®Google Scholar
• Tseng, S. F., Z. J. Shen, H. J. Tsai, Y. H. Lin, and S. C. Teng. 2009. Rapid Cdc13 turnover and telomere length homeostasis are controlled by Cdk1-mediated phosphorylation of Cdc13. Nucleic Acids Res. 37:3602–3611.
   PubMedGoogle Scholar
• Venteicher, A. S., E. B. Abreu, Z. Meng, K. E. McCann, R. M. Terns, T. D. Veenstra, M. P. Terns, and S. E. Artandi. 2009. A human telomerase holoenzyme protein required for Cajal body localization and telomere synthesis. Science 323:644–648.
   PubMed Web of Science ®Google Scholar
• Vulliamy, T. J., and I. Dokal. 2008. Dyskeratosis congenita: the diverse clinical presentation of mutations in the telomerase complex. Biochimie 90:122–130.
   PubMed Web of Science ®Google Scholar
• Wang, F., E. R. Podell, A. J. Zaug, Y. Yang, P. Baciu, T. R. Cech, and M. Lei. 2007. The POT1-TPP1 telomere complex is a telomerase processivity factor. Nature 445:506–510.
   PubMed Web of Science ®Google Scholar
• Weinrich, S. L., R. Pruzan, L. Ma, M. Ouellette, V. M. Tesmer, S. E. Holt, A. G. Bodnar, S. Lichtsteiner, N. W. Kim, J. B. Trager, R. D. Taylor, R. Carlos, W. H. Andrews, W. E. Wright, J. W. Shay, C. B. Harley, and G. B. Morin. 1997. Reconstitution of human telomerase with the template RNA component hTR and the catalytic protein subunit hTRT. Nat. Genet. 17:498–502.
   PubMed Web of Science ®Google Scholar
• Wenz, C., B. Enenkel, M. Amacker, C. Kelleher, K. Damm, and J. Lingner. 2001. Human telomerase contains two cooperating telomerase RNA molecules. EMBO J. 20:3526–3534.
   PubMed Web of Science ®Google Scholar
• Xin, H., D. Liu, and Z. Songyang. 2008. The telosome/shelterin complex and its functions. Genome Biol. 9:232.
   PubMedGoogle Scholar
• Xin, H., D. Liu, M. Wan, A. Safari, H. Kim, W. Sun, M. S. O'Connor, and Z. Songyang. 2007. TPP1 is a homologue of ciliate TEBP-beta and interacts with POT1 to recruit telomerase. Nature 445:559–562.
   PubMed Web of Science ®Google Scholar
• Ye, J. Z., and T. de Lange. 2004. TIN2 is a tankyrase 1 PARP modulator in the TRF1 telomere length control complex. Nat. Genet. 36:618–623.
   PubMed Web of Science ®Google Scholar
• Ye, J. Z., D. Hockemeyer, A. N. Krutchinsky, D. Loayza, S. M. Hooper, B. T. Chait, and T. de Lange. 2004. POT1-interacting protein PIP1: a telomere length regulator that recruits POT1 to the TIN2/TRF1 complex. Genes Dev. 18:1649–1654.
   PubMed Web of Science ®Google Scholar
• Yehezkel, S., Y. Segev, E. Viegas-Pequignot, K. Skorecki, and S. Selig. 2008. Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions. Hum. Mol. Genet. 17:2776–2789.
   PubMed Web of Science ®Google Scholar
• Zhu, Y., R. L. Tomlinson, A. A. Lukowiak, R. M. Terns, and M. P. Terns. 2004. Telomerase RNA accumulates in Cajal bodies in human cancer cells. Mol. Biol. Cell 15:81–90.
   PubMed Web of Science ®Google Scholar