Involvement of SRSF11 in cell cycle-specific recruitment of telomerase to telomeres at nuclear speckles

Nucleic Acids Research

Volumn 43, Issue 17, 2015, Pages 8435-8451

  Lee, Ji Hoon ^a   Jeong, Sun Ah ^a   Khadka, Prabhat ^a   Hong, Juyeong ^a   Chung, In Kwon ^a  

^a Yonsei University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; MESSENGER RNA PRECURSOR; SRSF11 PROTEIN; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG; RNA; SERINE ARGININE RICH SPLICING FACTOR; SFRS11 PROTEIN, HUMAN; TELOMERASE RNA; TELOMERIC REPEAT BINDING FACTOR 2;

AFFINITY CHROMATOGRAPHY; ARTICLE; CELL CYCLE; CELL CYCLE S PHASE; CELL DIVISION; CELL NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVITY; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; RNA SPLICING; TANDEM MASS SPECTROMETRY; TELOMERE; TELOMERE ELONGATION; CHEMISTRY; ENZYMOLOGY; GENETICS; HELA CELL LINE; METABOLISM; TELOMERE HOMEOSTASIS; TUMOR CELL LINE;

CELL CYCLE; CELL LINE, TUMOR; CELL NUCLEUS STRUCTURES; HELA CELLS; HUMANS; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA; SERINE-ARGININE SPLICING FACTORS; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS; TELOMERIC REPEAT BINDING PROTEIN 2;

EID: 84949009414     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv844     Document Type: Article

References (52)

1. Blackburn, E.H. (2001) Switching and signaling at the telomere. Cell, 106, 661-673.
2. Smogorzewska, A. and de Lange, T. (2004) Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem., 73, 177-208.
3. Liu, D., O'Connor, M.S., Qin, J. and Songyang, Z. (2004) Telosome, a mammalian telomere-associated complex formed by multiple telomeric proteins. J. Biol. Chem., 279, 51338-51342.
4. de Lange, T. (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev., 19, 2100-2110.
5. Palm, W. and de Lange, T. (2008) How shelterin protects mammalian telomeres. Annu. Rev. Genet., 42: 301-334.
6. Sfeir, A. and de Lange, T. (2012) Removal of shelterin reveals the telomere end-protection problem. Science, 336, 593-597.
7. Bryan, T.M., Englezou, A., Dalla-Pozza, L., Dunham, M.A. and Reddel, R.R. (1997) Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med., 3, 1271-1274.
8. Dunham, M.A., Neumann, A.A., Fasching, C.L. and Reddel, R.R. (2000) Telomere maintenance by recombination in human cells. Nat. Genet., 26, 447-450.
9. Autexier, C. and Lue, N.F. (2006) The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem., 75, 493-517.
10. Bianchi, A. and Shore, D. (2008) How telomerase reaches its end: mechanism of telomerase regulation by the telomeric complex. Mol. Cell, 31, 153-165.
11. Kim, N.W., Piatyszek, M.A., Prowse, K.R., Harley, C.B., West, M.D., Ho, P.L., Coviello, G.M., Wright, W.E., Weinrich, S.L. and Shay, J.W. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science, 266, 2011-2015.
12. Bodnar, A.G., Ouellette, M., Frolkis, M., Holt, S.E., Chiu, C.P., Morin, G.B., Harley, C.B., Shay, J.W., Lichtsteiner, S. and Wright, WE. (1998) Extension of life-span by introduction of telomerase into normal human cells. Science, 279, 349-352.
13. Hahn, W.C., Counter, C.M., Lundberg, A.S., Beijersbergen, R.L., Brooks, M.W. and Weinberg, R.A. (1999) Creation of human tumor cells with defined genetic elements. Nature, 400, 464-468.
14. Darzacq, X., Kittur, N., Roy, S., Shav-Tal, Y., Singer, R.H. and Meier, U.T. (2006) Stepwise RNP assembly at the site of H/ACA RNA transcription in human cells. J. Cell Biol., 173, 207-218.
15. Egan, E.D. and Collins, K. (2012) Biogenesis of telomerase ribonucleoproteins. RNA, 18, 1747-1759.
16. Richard, P., Kiss, A.M., Darzacq, X. and Kiss, T. (2006) Cotranscriptional recognition of human intronic box H/ACA snoRNAs occurs in a splicing-independent manner. Mol. Cell. Biol., 26, 2540-2549.
17. Wang, C. and Meier, U.T. (2004) Architecture and assembly of mammalian H/ACA small nucleolar and telomerase ribonucleoproteins. EMBO J., 23, 1857-1867.
18. Cristofari, G., Adolf, E., Reichenbach, P., Sikora, K., Terns, R.M., Terns, M.P. and Lingner, J. (2007) Human telomerase RNA accumulation in Cajal bodies facilitates telomerase recruitment to telomeres and telomere elongation. Mol. Cell, 27, 882-889.
19. Tycowski, K.T., Shu, M.D., Kukoyi, A. and Steitz, J.A. (2009) A conserved WD40 protein binds the Cajal body localization signal of scaRNP particles. Mol. Cell, 34, 47-57.
20. Venteicher, A.S., Abreu, E.B., Meng, Z., McCann, K.E., Terns, R.M., Veenstra, T.D., Terns, M.P. and Artandi, S.E. (2009) A human telomerase holoenzyme protein required for Cajal body localization and telomere synthesis. Science, 323, 644-648.
21. Venteicher, A.S. and Artandi, S.E. (2009) TCAB1: driving telomerase to Cajal bodies. Cell Cycle, 8, 1329-1331.
22. Lee, J.H., Lee, Y.S., Jeong, S.A., Khadka, P., Roth, J. and Chung, I.K. (2014) Catalytically active telomerase holoenzyme is assembled in the dense fibrillar component of the nucleolus during S phase. Histochem. Cell Biol., 141, 137-152.
23. Zhong, F.L., Batista, L.F., Freund, A., Pech, M.F., Venteicher, A.S. and Artandi, S.E. (2012) TPP1 OB-fold domain controls telomere maintenance by recruiting telomerase to chromosome ends. Cell, 150, 481-494.
24. Nandakumar, J., Bell, C.F., Weidenfeld, I., Zaug, A.J., Leinwand, L.A. and Cech, T.R. (2012) The TEL patch of telomere protein TPP1 mediates telomerase recruitment and processivity. Nature, 492, 285-289.
25. Xin, H., Liu, D., Wan, M., Safari, A., Kim, H., Sun, W., O'Connor, M.S. and Songyang, Z. (2007) TPP1 is a homologue of ciliate TEBP-beta and interacts with POT1 to recruit telomerase. Nature, 445, 559-562.
26. Lamond, A.I. and Spector, D.L. (2003) Nuclear speckles: a model for nuclear organelles. Nat. Rev. Mol. Cell. Biol., 4, 605-612.
27. Huang, S. and Spector, D.L. (1992) U1 and U2 small nuclear RNAs are present in nuclear speckles. Proc. Natl. Acad. Sci., 89, 305-308.
28. Shepard, P.J. and Hertel, K.J. (2009) The SR protein family. Genome Biol., 10, 242.
29. Wu, J.Y., Kar, A., Kuo, D., Yu, B. and Havlioglu, N. (2006) SRp54 (SFRS11), a regulator for tau exon 10 alternative splicing identified by an expression cloning strategy. Mol. Cell. Biol., 26, 6739-6747.
30. Listerman, I., Sun, J., Gazzaniga, F.S., Lukas, J.L. and Blackburn, E.H. (2013) The major reverse transcriptase-incompetent splice variant of the human telomerase protein inhibits telomerase activity but protects from apoptosis. Cancer Res., 73, 2817-2828.
31. Lee, J.H., Khadka, P., Baek, S.H. and Chung, I.K. (2010) CHIP promotes human telomerase reverse transcriptase degradation and negatively regulates telomerase activity. J. Biol. Chem., 285, 42033-42045.
32. Lee, G.E., Yu, E.Y., Cho, C.H., Lee, J., Muller, M.T. and Chung, I.K. (2004) DNA-protein kinase catalytic subunit-interacting protein KIP binds telomerase by interacting with human telomerase reverse transcriptase. J. Biol. Chem., 279, 34750-34755.
33. Kim, J.H., Kim, J.H., Lee, G.E., Lee, J.E. and Chung, I.K. (2003) Potent inhibition of human telomerase by nitrostyrene derivatives. Mol. Pharmacol., 63, 1117-11124.
34. Kim, N.W. and Wu, F. (1997) Advances in quantification and characterization of telomerase activity by the telomeric repeat amplification protocol (TRAP). Nucleic Acids Res., 25, 2595-2597.
35. Abreu, E., Terns, R.M. and Terns, M.P. (2011) Visualization of human telomerase localization by fluorescence microscopy techniques. Methods Mol. Biol., 735, 125-137.
36. Her, Y.R. and Chung, I.K. (2013) p300-mediated acetylation of TRF2 is required for maintaining functional telomeres. Nucleic Acids Res., 41, 2267-2283.
37. Cristofari, G. and Lingner, J. (2006) Telomere length homeostasis requires that telomerase levels are limiting. EMBO J., 25, 565-574.
38. Mitchell, J.R., Wood, E. and Collins, K. (1999) A telomerase component is defective in the human disease dyskeratosis congenita. Nature, 402, 551-555.
39. Khurts, S., Masutomi, K., Delgermaa, L., Arai, K., Oishi, N., Mizuno, H., Hayashi, N., Hahn, W.C. and Murakami, S. (2004) Nucleolin interacts with telomerase. J. Biol. Chem., 279, 51508-51515.
40. Li, Y., Wang, X., Zhang, X. and Goodrich, D.W. (2005) Human hHpr1/p84/Thoc1 regulates transcriptional elongation and physically links RNA polymerase II and RNA processing factors. Mol. Cell. Biol., 25, 4023-4033.
41. Venteicher, A.S., Meng, Z., Mason, P.J., Veenstra, T.D. and Artandi, S.E. (2008) Identification of ATPases pontin and reptin as telomerase components essential for holoenzyme assembly. Cell, 132, 945-957.
42. Jegou, T., Chung, I., Heuvelman, G., Wachsmuth, M., Görisch, S.M., Greulich-Bode, K.M., Boukamp, P., Lichter, P. and Rippe, K. (2009) Dynamics of telomeres and promyelocytic leukemia nuclear bodies in a telomerase-negative human cell line. Mol. Biol. Cell, 20, 2070-2082.
43. Tomlinson, R.L., Ziegler, T.D., Supakorndej, T., Terns, R.M. and Terns, M.P. (2006) Cell cycle-regulated trafficking of human telomerase to telomeres. Mol. Biol. Cell, 17, 955-965.
44. Wu, J.Y., Kar, A., Kuo, D., Yu, B. and Havlioglu, N. (2006) SRp54 (SFRS11), a regulator for tau exon 10 alternative splicing identified by an expression cloning strategy. Mol. Cell. Biol., 26, 6739-6747.
45. Sharma, A., Takata, H., Shibahara, K., Bubulya, A. and Bubulya, P.A. (2010) Son is essential for nuclear speckle organization and cell cycle progression. Mol. Biol. Cell, 21, 650-663.
46. Tomlinson, R.L., Abreu, E.B., Ziegler, T., Ly, H., Counter, C.M., Terns, R.M. and Terns, M.P. (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.
47. 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.
48. Jády, 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.
49. Vulliamy, T., Marrone, A., Goldman, F., Dearlove, A., Bessler, M., Mason, P.J. and Dokal, I. (2001) The RNA component of telomerase is mutated in autosomal dominant dyskeratosis congenita. Nature, 413, 432-435.
50. Savage, S.A. and Alter, B.P. (2008) The role of telomere biology in bone marrow failure and other disorders. Mech. Ageing Dev., 129, 35-47.
51. Calado, R.T., Regal, J.A., Kajigaya, S. and Young, N.S. (2009) Erosion of telomeric single-stranded overhang in patients with aplastic anaemia carrying telomerase complex mutations. Eur. J. Clin. Invest., 39, 1025-1032.
52. Zhong, F., Savage, S.A., Shkreli, M., Giri, N., Jessop, L., Myers, T., Chen, R., Alter, B.P. and Artandi, S.E. (2011) Disruption of telomerase trafficking by TCAB1 mutation causes dyskeratosis congenita. Genes Dev., 25, 11-16.