Cell cycle-regulated trafficking of human telomerase to telomeres

Molecular Biology of the Cell

Volumn 17, Issue 2, 2006, Pages 955-965

  Tomlinson, Rebecca L ^a   Ziegler, Tania D ^a   Supakorndej, Teerawit ^a   Terns, Rebecca M ^a   Terns, Michael P ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TELOMERASE RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELLULAR DISTRIBUTION; COILED BODY; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME REGULATION; HELA CELL; HUMAN; HUMAN CELL; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; TELOMERE;

CELL CYCLE; CELL NUCLEOLUS; COILED BODIES; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; MODELS, BIOLOGICAL; PROTEIN TRANSPORT; RNA, UNTRANSLATED; S PHASE; TELOMERASE; TELOMERE;

EID: 31944444988     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-09-0903     Document Type: Article

References (58)

1. Andrade, L. E., Tan, E. M., and Chan, E. K. (1993). Immunocytochemical analysis of the coiled body in the cell cycle and during cell proliferation. Proc. Natl. Acad. Sci. USA 90, 1947-1951.
2. Bachand, F., Boisvert, F. M., Cote, J., Richard, S., and Autexier, C. (2002). The product of the survival of motor neuron (SMN) gene is a human telomerase-associated protein. Mol. Biol. Cell 13, 3192-3202.
3. Blasco, M. A. (2005). Mice with bad ends: mouse models for the study of telomeres and telomerase in cancer and aging. EMBO J. 24, 1095-1103.
4. Cioce, M., and Lamond, A. I. (2005). Cajal bodies: a long history of discovery. Annu. Rev. Cell Dev. Biol. 21, 105-131.
5. Colgin, L., and Reddel, R. (2004). Telomere biology: a new player in the end zone. Curr. Biol. 14, R901-R902.
6. Collins, K., and Mitchell, J. R. (2002). Telomerase in the human organism. Oncogene 21, 564-579.
7. Cong, Y. S., Wright, W. E., and Shay, J. W. (2002). Human telomerase and its regulation. Microbiol. Mol. Biol. Rev. 66, 407-425.
8. de Lange, T. (2002). Protection of mammalian telomeres. Oncogene 21, 532-540.
9. Etheridge, K. T., Banik, S. S., Armbruster, B. N., Zhu, Y., Terns, R. M., Terns, M. P., and Counter, C. M. (2002). The nucleolar localization domain of the catalytic subunit of human telomerase. J. Biol. Chem. 277, 24764-24770.
10. Fang, G., and Cech, T. R. (1995). Telomerase RNA localized in the replication band and spherical subnuclear organelles in hypotrichous ciliates. J. Cell Biol. 130, 243-253.
11. Frey, M. R., and Matera, A. G. (1995). Coiled bodies contain U7 small nuclear RNA and associate with specific DNA sequences in interphase human cells. Proc. Natl. Acad. Sci. USA 92, 5915-5919.
12. Gall, J. G. (2000). Cajal bodies: the first 100 years. Annu. Rev. Cell Dev. Biol. 16, 273-300.
13. Gall, J. G. (2003). The centennial of the Cajal body. Nat. Rev. Mol. Cell. Biol. 4, 975-980.
14. Greider, C. W., and Blackburn, E. H. (1989). A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337, 331-337.
15. Gubitz, A. K., Feng, W., and Dreyfuss, G. (2004). The SMN complex. Exp. Cell Res. 296, 51-56.
16. Harley, C. B., Futcher, A. B., and Greider, C. W. (1990). Telomeres shorten during ageing of human fibroblasts. Nature 345, 458-460.
17. Harrington, L. (2004). Those dam-aged telomeres! Curr. Opin. Genet. Dev. 14, 22-28.
18. Holt, S. E., Aisner, D. L., Shay, J. W., and Wright, W. E. (1997). Lack of cell cycle regulation of telomerase activity in human cells. Proc. Natl. Acad. Sci. USA 94, 10687-10692.
19. Jady, B. E., Bertrand, E., and 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.
20. Kim, J. H., Park, S. M., Kang, M. R., Oh, S. Y., Lee, T. H., Muller, M. T., and Chung, I. K. (2005). Ubiquitin ligase MKRN1 modulates telomere length homeostasis through a proteolysis of hTERT. Genes Dev. 19, 776-781.
21. Lam, Y. W., Trinkle-Mulcahy, L., and Lamond, A. I. (2005). The nucleolus. J. Cell Sci. 118, 1335-1337.
22. Liu, Q., and Dreyfuss, G. (1996). A novel nuclear structure containing the survival of motor neurons protein. EMBO J. 15, 3555-3565.
23. 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.
24. Lukowiak, A. A., Narayanan, A., Li, Z. H., Terns, R. M., and Terns, M. P. (2001). The snoRNA domain of vertebrate telomerase RNA functions to localize the RNA within the nucleus. RNA 7, 1833-1844.
25. Ma, T., Van Tine, B. A., Wei, Y., Garrett, M. D., Nelson, D., Adams, P. D., Wang, J., Qin, J., Chow, L. T., and Harper, J. W. (2000). Cell cycle-regulated phosphorylation of p220(NPAT) by cyclin E/Cdk2 in Cajal bodies promotes histone gene transcription. Genes Dev. 14, 2298-2313.
26. Masutomi, K., et al. (2003). Telomerase maintains telomere structure in normal human cells. Cell 114, 241-253.
27. McEachern, M. J., Krauskopf, A., and Blackburn, E. H. (2000). Telomeres and their control. Annu. Rev. Genet. 34, 331-358.
28. Miele, A., et al (2005). HiNF-P directly links the cyclin E/CDK2/p220NPAT pathway to histone H4 gene regulation at the G1/S phase cell cycle transition. Mol. Cell. Biol. 25, 6140-6153.
29. Mili, S., and Steitz, J. A. (2004). Evidence for reassociation of RNA-binding proteins after cell lysis: implications for the interpretation of immunoprecipitation analyses. RNA 10, 1692-1694.
30. Mitchell, J. R., Cheng, J., and 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.
31. Molenaar, C., Wiesmeijer, K., Verwoerd, N. P., Khazen, S., Eils, R., Tanke, H. J., and Dirks, R. W. (2003). Visualizing telomere dynamics in living mammalian cells using PNA probes. EMBO J. 22, 6631-6641.
32. O'Keefe, R. T., Henderson, S. C., and Spector, D. L. (1992). Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosome-specific alpha-satellite DNA sequences. J. Cell Biol. 116, 1095-1110.
33. Olson, M. O., Dundr, M., and Szebeni, A. (2000). The nucleolus: an old factory with unexpected capabilities. Trends Cell Biol. 10, 189-196.
34. Ouellette, M. M., Aisner, D. L., Savre-Train, I., Wright, W. E., and Shay, J. W. (1999). Telomerase activity does not always imply telomere maintenance. Biochem. Biophys. Res. Commun. 254, 795-803.
35. Ouellette, M. M., Liao, M., Herbert, B. S., Johnson, M., Holt, S. E., Liss, H. S., Shay, J. W., and Wright, W. E. (2000). Subsenescent telomere lengths in fibroblasts immortalized by limiting amounts of telomerase. J. Biol. Chem. 275, 10072-10076.
36. Pederson, T. (1998). The plurifunctional nucleolus. Nucleic Acids Res. 26, 3871-3876.
37. Platani, M., Goldberg, I., Swedlow, J. R., and Lamond, A. I. (2000). In vivo analysis of Cajal body movement, separation, and joining in live human cells. J. Cell Biol. 151, 1561-1574.
38. Schul, W., van Der Kraan, I., Matera, A. G., van Driel, R., and de Jong, L. (1999). Nuclear domains enriched in RNA 3′-processing factors associate with coiled bodies and histone genes in a cell cycle-dependent manner. Mol. Biol. Cell 10, 3815-3824.
39. Shay, J. W., and Bacchetti, S. (1997). A survey of telomerase activity in human cancer. Eur. J. Cancer 33, 787-791.
40. Shopland, L. S., Byron, M., Stein, J. L., Lian, J. B., Stein, G. S., and Lawrence, J. B. (2001). Replication-dependent histone gene expression is related to Cajal body (CB) association but does not require sustained CB contact. Mol. Biol. Cell 12, 565-576.
41. Sleeman, J. E., Trinkle-Mulcahy, L., Prescott, A. R., Ogg, S. C., and Lamond, A. I. (2003). Cajal body proteins SMN and Coilin show differential dynamic behaviour in vivo. J. Cell Sci. 116, 2039-2050.
42. Smogorzewska, A., and de Lange, T. (2004). Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem. 73, 177-208.
43. Sprung, C. N., Reynolds, G. E., Jasin, M., and Murnane, J. P. (1999). Chromosome healing in mouse embryonic stem cells. Proc. Natl. Acad. Sci. USA 96, 6781-6786.
44. Taggart, A. K., Teng, S. C., and Zakian, V. A. (2002). Est1p as a cell cycle-regulated activator of telomere-bound telomerase. Science 297, 1023-1026.
45. Teixeira, M. T., Arneric, M., Sperisen, P., and Lingner, J. (2004). Telomere length homeostasis is achieved via a switch between telomerase-extendible and -nonextendible states. Cell 117, 323-335.
46. Ten Hagen, K. G., Gilbert, D. M., Willard, H. F., and Cohen, S. N. (1990). Replication timing of DNA sequences associated with human centromeres and telomeres. Mol. Cell. Biol. 10, 6348-6355.
47. Terns, M. P., and Terns, R. M. (2001). Macromolecular complexes: SMN-the master assembler. Curr. Biol. 21, R862-R864.
48. Whitehead, S. E., Jones, K. W., Zhang, X., Cheng, X., Terns, R. M., and Terns, M. P. (2002). Determinants of the interaction of the spinal muscular atrophy disease protein SMN with the dimethylarginine-modified box H/ACA small nucleolar ribonucleoprotein GAR1. J. Biol. Chem. 277, 48087-48093.
49. Wong, J. M., Kusdra, L., and Collins, K. (2002). Subnuclear shuttling of human telomerase induced by transformation and DNA damage. Nat. Cell Biol. 4, 731-736.
50. Woodfine, K., Fiegler, H., Beare, D. M., Collins, J. E., McCann, O. T., Young, B. D., Debernardi, S., Mott, R., Dunham, I., and Carter, N. P. (2004). Replication timing of the human genome. Hum. Mol. Genet. 13, 191-202.
51. Wright, W. E., Tesmer, V. M., Liao, M. L., and Shay, J. W. (1999). Normal human telomeres are not late replicating. Exp. Cell Res. 251, 492-499.
52. Yang, S. W., Tin, E., Chung, I. K., and Kim, W. T. (2002a). Cell cycle-dependent regulation of telomerase activity by auxin, abscisic acid and protein phosphorylation in tobacco BY-2 suspension culture cells. Plant J. 29, 617-626.
53. Yang, Y., Chen, Y., Zhang, C., Huang, H., and Weissman, S. M. (2002b). Nucleolar localization of hTERT protein is associated with telomerase function. Exp. Cell Res. 277, 201-209.
54. Yannoni, Y. M., and White, K. (1997). Association of the neuron-specific RNA binding domain-containing protein ELAV with the coiled body in Drosophila neurons. Chromosoma 105, 332-341.
55. Zhao, J., Kennedy, B. K., Lawrence, B. D., Barbie, D. A., Matera, A. G., Fletcher, J. A., and Harlow, E. (2000). NPAT links cyclin E-Cdk2 to the regulation of replication-dependent histone gene transcription. Genes Dev. 14, 2283-2297.
56. Zhu, X., Kumar, R., Mandai, M., Sharma, N., Sharma, H. W., Dhingra, U., Sokoloski, J. A., Hsiao, R., and Narayanan, R. (1996). Cell cycle-dependent modulation of telomerase activity in tumor cells. Proc. Natl. Acad. Sci. USA 93, 6091-6095.
57. Zhu, Y., Tomlinson, R. L., Lukowiak, A. A., Terns, R. M., and Terns, M. P. (2004). Telomerase RNA accumulates in Cajal bodies in human cancer cells. Mol. Biol. Cell 15, 81-90.
58. Zou, Y., Gryaznov, S. M., Shay, J. W., Wright, W. E., and Cornforth, M. N. (2004). Asynchronous replication timing of telomeres at opposite arms of mammalian chromosomes. Proc. Natl. Acad. Sci. USA 101, 12928-12933.