Biogenesis of telomerase ribonucleoproteins

RNA

Volumn 18, Issue 10, 2012, Pages 1747-1759

  Egan, Emily D ^a   Collins, Kathleen ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ribonucleoprotein biogenesis; Telomerase holoenzyme; Telomerase reverse transcriptase; Telomerase RNA; Telomere maintenance

Indexed keywords

DYSKERIN; PROTEIN P19; PROTEIN P50; PROTEIN P75; PROTEIN SM; REPLICATION FACTOR A; RIBONUCLEOPROTEIN; SYNAPTOTAGMIN I; TEB1 PROTEIN; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TELOMERASE RNA; UNCLASSIFIED DRUG;

BIOGENESIS; CATALYSIS; CELL CYCLE S PHASE; CELL MIGRATION; ENZYME REGULATION; HUMAN; INTRON; KLUYVEROMYCES LACTIS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; RNA STRUCTURE; RNA TRANSPORT; SACCHAROMYCES CEREVISIAE; TELOMERE; TETRAHYMENA THERMOPHILA; VERTEBRATE;

ANIMALS; CILIOPHORA; HUMANS; MODELS, BIOLOGICAL; NUCLEIC ACID CONFORMATION; PROTEIN MULTIMERIZATION; RIBONUCLEOPROTEINS; TELOMERASE; YEASTS;

CILIOPHORA; EUKARYOTA; VERTEBRATA;

EID: 84866611481     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.034629.112     Document Type: Review

References (171)

1. Abreu E, Aritonovska E, Reichenbach P, Cristofari G, Culp B, Terns RM, Lingner J, Terns MP. 2010. TIN2-tethered TPP1 recruits human telomerase to telomeres in vivo. Mol Cell Biol 30: 2971-2982.
2. Akiyama BM, Loper J, Najarro K, Stone MD. 2012. The C-terminal domain of Tetrahymena thermophila telomerase holoenzyme protein p65 induces multiple structural changes in telomerase RNA. RNA 18: 653-660.
3. Armanios M. 2009. Syndromes of telomere shortening. Annu Rev Genomics Hum Genet 10: 45-61.
4. Autexier C, Greider CW. 1995. Boundary elements of the Tetrahymena telomerase RNA template and alignment domains. Genes Dev 9: 2227-2239.
5. Autexier C, Lue NF. 2006. The structure and function of telomerase reverse transcriptase. Annu Rev Biochem 75: 493-517.
6. Bachand F, Boisvert FM, Cote J, Richard S, 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.
7. Beernink HT, Miller K, Deshpande A, Bucher P, Cooper JP. 2003. Telomere maintenance in fission yeast requires an Est1 ortholog. Curr Biol 13: 575-580.
8. Belfort M, Curcio MJ, Lue NF. 2011. Telomerase and retrotransposons: Reverse transcriptases that shaped genomes. Proc Natl Acad Sci 108: 20304-20310.
9. Berman AJ, Gooding AR, Cech TR. 2010. Tetrahymena telomerase protein p65 induces conformational changes throughout telomerase RNA (TER) and rescues telomerase reverse transcriptase and TER assembly mutants. Mol Cell Biol 30: 4965-4976.
10. Blackburn EH, Collins K. 2011. Telomerase: An RNP enzyme synthesizes DNA. Cold Spring Harb Perspect Biol 3: a003558. doi: 10.1101/cshperspect.a003558.
11. Blackburn EH, Greider CW, Szostak JW. 2006. Telomeres and telomerase: The path from maize, Tetrahymena and yeast to human cancer and aging. Nat Med 12: 1133-1138.
12. Bosoy D, Peng Y, Mian IS, Lue NF. 2003. Conserved N-terminal motifs of telomerase reverse transcriptase required for ribonucleoprotein assembly in vivo. J Biol Chem 278: 3882-3890.
13. Boulon S, Verheggen C, Jady BE, Girard C, Pescia C, Paul C, Ospina JK, Kiss T, Matera AG, Bordonne R, et al. 2004. PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell 16: 777-787.
14. Boulon S, Marmier-Gourrier N, Pradet-Balade B, Wurth L, Verheggen C, Jady BE, Rothe B, Pescia C, Robert MC, Kiss T, et al. 2008. The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J Cell Biol 180: 579-595.
15. Box JA, Bunch JT, Tang W, Baumann P. 2008a. Spliceosomal cleavage generates the 39 end of telomerase RNA. Nature 456: 910-914.
16. Box JA, Bunch JT, Zappulla DC, Glynn EF, Baumann P. 2008b. A flexible template boundary element in the RNA subunit of fission yeast telomerase. J Biol Chem 283: 24224-24233.
17. Brown Y, Abraham M, Pearl S, Kabaha MM, Elboher E, Tzfati Y. 2007. A critical three-way junction is conserved in budding yeast and vertebrate telomerase RNAs. Nucleic Acids Res 35: 6280-6289.
18. Chai W, Ford LP, Lenertz L, Wright WE, Shay JW. 2002. Human Ku70/80 associates physically with telomerase through interaction with hTERT. J Biol Chem 277: 47242-47247.
19. 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.
20. Chapon C, Cech T, Zaug A. 1997. Polyadenylation of telomerase RNA in budding yeast. RNA 3: 1337-1351.
21. Chen JL, Blasco MA, Greider CW. 2000. Secondary structure of vertebrate telomerase RNA. Cell 100: 503-514.
22. Chen JL, Opperman KK, Greider CW. 2002. A critical stem-loop structure in the CR4-CR5 domain of mammalian telomerase RNA. Nucleic Acids Res 30: 592-597.
23. Cifuentes-Rojas C, Kannan K, Tseng L, Shippen DE. 2011. Two RNA subunits and POT1a are components of Arabidopsis telomerase. Proc Natl Acad Sci 108: 73-78.
24. Collins K. 1999. Ciliate telomerase biochemistry. Annu Rev Biochem 68: 187-218.
25. Collins K. 2008. Physiological assembly and activity of human telomerase complexes. Mech Ageing Dev 129: 91-98.
26. Collins K. 2009. Forms and functions of telomerase RNA. In Non-protein coding RNAs, Vol. 13 (ed. NG Walter et al.), pp. 285-301. Springer-Verlag, Berlin, Germany.
27. Collins K. 2011. Single-stranded DNA repeat synthesis by telomerase. Curr Opin Chem Biol 15: 643-648.
28. Cristofari G, Adolf E, Reichenbach P, Sikora K, Terns RM, Terns MP, Lingner J. 2007. Human telomerase RNA accumulation in Cajal bodies facilitates telomerase recruitment to telomeres and telomere elongation. Mol Cell 27: 882-889.
29. Cunningham DD, Collins K. 2005. Biological and biochemical functions of RNA in the Tetrahymena telomerase holoenzyme. Mol Cell Biol 25: 4442-4454.
30. Darzacq X, Kittur N, Roy S, Shav-Tal Y, Singer RH, Meier UT. 2006. Stepwise RNP assembly at the site of H/ACA RNA transcription in human cells. J Cell Biol 173: 207-218.
31. de Lange T. 2010. How shelterin solves the telomere end-protection problem. Cold Spring Harb Symp Quant Biol 75: 167-177.
32. DeZwaan DC, Freeman BC. 2010. Is there a telomere-bound 'EST'telomerase holoenzyme? Cell Cycle 9: 1913-1917.
33. Eckert B, Collins K. 2012. Roles of telomerase reverse transcriptase N-terminal domain in assembly and activity of Tetrahymena telomerase holoenzyme. J Biol Chem 287: 12805-12814.
34. Egan ED, Collins K. 2010. Specificity and stoichiometry of subunit interactions in the human telomerase holoenzyme assembled in vivo. Mol Cell Biol 30: 2775-2786.
35. Egan ED, Collins K. 2012. An enhanced H/ACA RNP assembly mechanism for human telomerase RNA. Mol Cell Biol 32: 2428-2439.
36. Feng J, Funk WD, Wang S, Weinrich SL, Avilion AA, Chiu C, Adams RR, Chang E, Allsopp RC, Yu J, et al. 1995. The RNA component of human telomerase. Science 269: 1236-1241.
37. Ferrezuelo F, Steiner B, Aldea M, Futcher B. 2002. Biogenesis of yeast telomerase depends on the importin Mtr10. Mol Cell Biol 22: 6046-6055.
38. Fisher TS, Zakian VA. 2005. Ku: A multifuntional protein involved in telomere maintenance. DNA Repair (Amst) 4: 1215-1226.
39. Fisher TS, Taggart AK, Zakian VA. 2004. Cell cycle-dependent regulation of yeast telomerase by Ku. Nat Struct Mol Biol 11: 1198-1205.
40. Forsythe HL, Jarvis JL, Turner JW, Elmore LW, Holt SE. 2001. Stable association of hsp90 and p23, but not hsp70, with active human telomerase. J Biol Chem 276: 15571-15574.
41. Fu D, Collins K. 2003. Distinct biogenesis pathways for human telomerase RNA and H/ACA small nucleolar RNAs. Mol Cell 11: 1361-1372.
42. Fu D, Collins K. 2006. Human telomerase and Cajal body ribonucleoproteins share a unique specificity of Sm protein association. Genes Dev 20: 531-536.
43. Fu D, Collins K. 2007. Purification of human telomerase complexes identifies factors involved in telomerase biogenesis and telomere length regulation. Mol Cell 28: 773-785.
44. 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.
45. Gallardo F, Laterreur N, Cusanelli E, Ouenzar F, Querido E, Wellinger RJ, 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.
46. 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.
47. Gilley D, Blackburn EH. 1999. The telomerase RNA pseudoknot is critical for the stable assembly of a catalytically active ribonucleo-protein. Proc Natl Acad Sci 96: 6621-6625.
48. Gillis AJ, Schuller AP, Skordalakes E. 2008. Structure of the Tribolium castaneum telomerase catalytic subunit TERT. Nature 455: 633-637.
49. Girard C, Verheggen C, Neel H, Cammas A, Vagner S, Soret J, Bertrand E, Bordonne R. 2008. Characterization of a short isoform of human Tgs1 hypermethylase associating with small nucleolar ribonucleoprotein core proteins and produced by limited proteolytic processing. J Biol Chem 283: 2060-2069.
50. Gomes NM, Shay JW, Wright WE. 2010. Telomere biology in metazoa. FEBS Lett 584: 3741-3751.
51. Grandin N, Damon C, Charbonneau M. 2001. Ten1 functions in telomere end protection and length regulation in association with Stn1 and Cdc13. EMBO J 20: 1173-1183.
52. Greider CW. 1991. Telomerase is processive. Mol Cell Biol 11: 4572-4580.
53. Greider CW, Blackburn EH. 1989. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337: 331-337.
54. Grozdanov PN, Roy S, Kittur N, Meier UT. 2009. SHQ1 is required prior to NAF1 for assembly of H/ACA small nucleolar and telomerase RNPs. RNA 15: 1188-1197.
55. Gunisova S, Elboher E, Nosek J, Gorkovoy V, Brown Y, Lucier JF, Laterreur N, Wellinger RJ, Tzfati Y, Tomaska L. 2009. Identification and comparative analysis of telomerase RNAs from Candida species reveal conservation of functional elements. RNA 15: 546-559.
56. Hinkley C, Blasco M, Funk W, Feng J, Villeponteau B, Greider C, Herr W. 1998. The mouse telomerase RNA 59-end lies just upstream of the telomerase template sequence. Nucleic Acids Res 26: 532-536.
57. Hoareau-Aveilla C, Bonoli M, Caizergues-Ferrer M, Henry Y. 2006. hNaf1 is required for accumulation of human box H/ACA snoRNPs, scaRNPs, and telomerase. RNA 12: 832-840.
58. Holt SE, Aisner DL, Baur J, Tesmer VM, Dy M, Ouellette M, Trager JB, Morin GB, Toft DO, Shay JW, et al. 1999. Functional requirement of p23 and Hsp90 in telomerase complexes. Genes Dev 13: 817-826.
59. Hsu HL, Gilley D, Blackburn EH, Chen DJ. 1999. Ku is associated with the telomere in mammals. Proc Natl Acad Sci 96: 12454-12458.
60. Hsu M, Yu EY, Singh SM, Lue NF. 2007. Mutual dependence of Candida albicans Est1p and Est3p in telomerase assembly and activation. Eukaryot Cell 6: 1330-1338.
61. Jacobs SA, Podell ER, Cech TR. 2006. Crystal structure of the essential N-terminal domain of telomerase reverse transcriptase. Nat Struct Mol Biol 13: 218-225.
62. Jády BE, 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.
63. Jády BE, Richard P, Bertrand E, Kiss T. 2006. Cell cycle-dependent recruitment of telomerase RNA and Cajal bodies to human telomeres. Mol Biol Cell 17: 944-954.
64. Jain D, Cooper JP. 2010. Telomeric strategies: Means to an end. Annu Rev Genet 44: 243-269.
65. Jamonnak N, Creamer TJ, Darby MM, Schaughency P, Wheelan SJ, Corden JL. 2011. Yeast Nrd1, Nab3, and Sen1 transcriptome-wide binding maps suggest multiple roles in post-transcriptional RNA processing. RNA 17: 2011-2025.
66. Kim JH, Park SM, Kang MR, Oh SY, Lee TH, Muller MT, Chung IK. 2005. Ubiquitin ligase MKRN1 modulates telomere length homeostasis through a proteolysis of hTERT. Genes Dev 19: 776-781.
67. Kiss T, Fayet-Lebaron E, Jády BE. 2010. Box H/ACA small ribonucleoproteins. Mol Cell 37: 597-606.
68. Kuehner JN, Pearson EL, Moore C. 2011. Unravelling the means to an end: RNA polymerase II transcription termination. Nat Rev Mol Cell Biol 12: 283-294.
69. Lai CK, Mitchell JR, Collins K. 2001. RNA binding domain of telomerase reverse transcriptase. Mol Cell Biol 21: 990-1000.
70. Lai CK, Miller MC, Collins K. 2002. Template boundary definition in Tetrahymena telomerase. Genes Dev 16: 415-420.
71. Latrick CM, Cech TR. 2010. POT1-TPP1 enhances telomerase processivity by slowing primer dissociation and aiding translocation. EMBO J 29: 924-933.
72. Lattmann S, Stadler MB, Vaughn JP, Akman SA, Nagamine Y. 2011. The DEAH-box RNA helicase RHAU binds an intramolecular RNA G-quadruplex in TERC and associates with telomerase holoenzyme. Nucleic Acids Res 39: 9390-9404.
73. Lee GE, Yu EY, Cho CH, Lee J, Muller MT, Chung IK. 2004. DNAprotein kinase catalytic subunit-interacting protein KIP binds telomerase by interacting with human telomerase reverse transcriptase. J Biol Chem 279: 34750-34755.
74. Lee J, Mandell EK, Rao T, Wuttke DS, Lundblad V. 2010. Investigating the role of the Est3 protein in yeast telomere replication. Nucleic Acids Res 38: 2279-2290.
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. Linger BR, Morin GB, Price CM. 2011. The Pot1a-associated proteins Tpt1 and Pat1 coordinate telomere protection and length regulation in Tetrahymena. Mol Biol Cell 22: 4161-4170.
77. Lingner J, Cech TR, Hughes TR, Lundblad V. 1997a. Three ever shorter telomere (EST) genes are dispensable for in vitro yeast telomerase activity. Proc Natl Acad Sci 94: 11190-11195.
78. Lingner J, Hughes TR, Shevchenko A, Mann M, Lundblad V, Cech TR. 1997b. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276: 561-567.
79. Livengood AJ, Zaug AJ, Cech TR. 2002. Essential regions of Saccharomyces cerevisiae telomerase RNA: Separate elements for Est1p and Est2p interaction. Mol Cell Biol 22: 2366-2374.
80. Ludérus ME, van Steensel B, Chong L, Sibon OC, Cremers FF, de Lange T. 1996. Structure, subnuclear distribution, and nuclear matrix association of the mammalian telomeric complex. J Cell Biol 135: 867-881.
81. Lue NF. 2010. Plasticity of telomere maintenance mechanisms in yeast. Trends Biochem Sci 35: 8-17.
82. Mihalusova M, Wu JY, Zhuang X. 2011. Functional importance of telomerase pseudoknot revealed by single-molecule analysis. Proc Natl Acad Sci 108: 20339-20344.
83. Miller MC, Collins K. 2002. Telomerase recognizes its template by using an adjacent RNA motif. Proc Natl Acad Sci 99: 6585-6590.
84. Min B, Collins K. 2009. An RPA-related sequence-specific DNA-binding subunit of telomerase holoenzyme is required for elongation processivity and telomere maintenance. Mol Cell 36: 609-619.
85. Min B, Collins K. 2010. Multiple mechanisms for elongation processivity within the reconstituted Tetrahymena telomerase holoenzyme. J Biol Chem 285: 16434-16443.
86. Mitchell JR, Collins K. 2000. Human telomerase activation requires two independent interactions between telomerase RNA and telomerase reverse transcriptase in vivo and in vitro. Mol Cell 6: 361-371.
87. Mitchell JR, Cheng J, Collins K. 1999. A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 39 end. Mol Cell Biol 19: 567-576.
88. Mitchell M, Gillis A, Futahashi M, Fujiwara H, Skordalakes E. 2010. Structural basis for telomerase catalytic subunit TERT binding to RNA template and telomeric DNA. Nat Struct Mol Biol 17: 513-518.
89. Moser BA, Nakamura TM. 2009. Protection and replication of telomeres in fission yeast. Biochem Cell Biol 87: 747-758.
90. ATR kinases promote Ccq1-Est1 interaction to maintain telomeres in fission yeast. Nat Struct Mol Biol 18: 1408-1413.
91. Mouaikel J, Verheggen C, Bertrand E, Tazi J, Bordonne R. 2002. Hypermethylation of the cap structure of both yeast snRNAs and snoRNAs requires a conserved methyltransferase that is localized to the nucleolus. Mol Cell 9: 891-901.
92. Mozdy AD, Podell ER, Cech TR. 2008. Multiple yeast genes, including Paf1 complex genes, affect telomere length via telomerase RNA abundance. Mol Cell Biol 28: 4152-4161.
93. Noël JF, Larose S, Abou Elela S, Wellinger RJ. 2012. Budding yeast telomerase RNA transcription termination is dictated by the Nrd1/Nab3 non-coding RNA termination pathway. Nucleic Acids Res 40: 5625-5636.
94. O'Connor CM, Collins K. 2006. A novel RNA binding domain in Tetrahymena telomerase p65 initiates hierarchical assembly of telomerase holoenzyme. Mol Cell Biol 26: 2029-2036.
95. O'Connor CM, Lai CK, Collins K. 2005. Two purified domains of telomerase reverse transcriptase reconstitute sequence-specific interactions with RNA. J Biol Chem 280: 17533-17539.
96. O'Sullivan RJ, Karlseder J. 2010. Telomeres: Protecting chromosomes against genome instability. Nat Rev Mol Cell Biol 11: 171-181.
97. Osterhage JL, Friedman KL. 2009. Chromosome end maintenance by telomerase. J Biol Chem 284: 16061-16065.
98. Osterhage JL, Talley JM, Friedman KL. 2006. Proteasome-dependent degradation of Est1p regulates the cell cycle-restricted assembly of telomerase in Saccharomyces cerevisiae. Nat Struct Mol Biol 13: 720-728.
99. Pardue ML, DeBaryshe PG. 2011. Retrotransposons that maintain chromosome ends. Proc Natl Acad Sci 108: 20317-20324.
100. Pennock E, Buckley K, Lundblad V. 2001. Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104: 387-396.
101. Peterson SE, Stellwagen AE, Diede SJ, Singer MS, Haimberger ZW, Johnson CO, Tzoneva M, Gottschling DE. 2001. The function of a stem-loop in telomerase RNA is linked to the DNA repair protein Ku. Nat Genet 27: 64-67.
102. Pfingsten JS, 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.
103. Podlevsky JD, Chen JJ. 2012. It all comes together at the ends: Telomerase structure, function, and biogenesis. Mutat Res 730: 3-11.
104. Prathapam R, Witkin KL, O'Connor CM, Collins K. 2005. A telomerase holoenzyme protein enhances telomerase RNA assembly with telomerase reverse transcriptase. Nat Struct Mol Biol 12: 252-257.
105. Qi H, Zakian VA. 2000. The Saccharomyces telomere-binding protein Cdc13p interacts with both the catalytic subunit of DNA polymerase a and the telomerase-associated Est1 protein. Genes Dev 14: 1777-1788.
106. Qi X, Xie M, Brown AF, Bley CJ, Podlevsky JD, Chen JJ. 2012. RNA/DNA hybrid binding affinity determines telomerase template-translocation efficiency. EMBO J 31: 150-161.
107. Qiao F, Cech TR. 2008. Triple-helix structure in telomerase RNA contributes to catalysis. Nat Struct Mol Biol 15: 634-640.
108. 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.
109. 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.
110. Richard P, Darzacq X, Bertrand E, Jády BE, Verheggen C, Kiss T. 2003. A common sequence motif determines the Cajal body-specific localization of box H/ACA scaRNAs. EMBO J 22: 4283-4293.
111. Richard P, Kiss AM, Darzacq X, Kiss T. 2006. Cotranscriptional recognition of human intronic box H/ACA snoRNAs occurs in a splicing-independent manner. Mol Cell Biol 26: 2540-2549.
112. Richards RJ, Wu H, Trantirek L, O'Connor CM, Collins K, Feigon J. 2006. Structural study of elements of Tetrahymena telomerase RNA stem-loop IV domain important for function. RNA 12: 1475-1485.
113. Robart AR, Collins K. 2010. Investigation of human telomerase holoenzyme assembly, activity, and processivity using disease-linked subunit variants. J Biol Chem 285: 4375-4386.
114. Robart AR, Collins K. 2011. Human telomerase domain interactions capture DNA for TEN domain-dependent processive elongation. Mol Cell 42: 308-318.
115. Robart AR, O'Connor CM, Collins K. 2010. Ciliate telomerase RNA loop IV nucleotides promote hierarchical RNP assembly and holoenzyme stability. RNA 16: 563-571.
116. Savage SA, Bertuch AA. 2010. The genetics and clinical manifestations of telomere biology disorders. Genet Med 12: 753-764.
117. Schoeftner S, Blasco MA. 2009. A 'higher order' of telomere regulation: telomere heterochromatin and telomeric RNAs. EMBO J 28: 2323-2336.
118. Seto AG, Zaug AJ, Sobel SG, Wolin SL, Cech TR. 1999. Saccharomyces cerevisiae telomerase is an Sm small nuclear ribonucleoprotein particle. Nature 401: 177-180.
119. Seto AG, Umansky K, Tzfati Y, Zaug AJ, Blackburn EH, Cech TR. 2003. A template-proximal RNA paired element contributes to Saccharomyces cerevisiae telomerase activity. RNA 9: 1323-1332.
120. Sexton AN, Collins K. 2011. The 59 guanosine tracts of human telomerase RNA are recognized by the G-quadruplex binding domain of the RNA helicase DHX36 and function to increase RNA accumulation. Mol Cell Biol 31: 736-743.
121. Singh M, Wang Z, Koo BK, Patel A, Cascio D, Collins K, Feigon J. 2012. Structural basis for telomerase RNA recognition and RNP assembly by the holoenzyme La family protein p65. Mol Cell 47: 16-26.
122. Snow BE, Erdmann N, Cruickshank J, Goldman H, Gill RM, Robinson MO, Harrington L. 2003. Functional conservation of the telomerase protein Est1p in humans. Curr Biol 13: 698-704.
123. Song K, Jung D, Jung Y, Lee SG, Lee I. 2000. Interaction of human Ku70 with TRF2. FEBS Lett 481: 81-85.
124. Stellwagen AE, Haimberger ZW, Veatch JR, Gottschling DE. 2003. Ku interacts with telomerase RNA to promote telomere addition at native and broken chromosome ends. Genes Dev 17: 2384-2395.
125. Stern JL, Bryan TM. 2008. Telomerase recruitment to telomeres. Cytogenet Genome Res 122: 243-254.
126. Stern JL, Zyner KG, Pickett HA, Cohen SB, Bryan TM. 2012. Telomerase recruitment requires both TCAB1 and Cajal bodies independently. Mol Cell Biol 32: 2384-2395.
127. Stewart JA, Chaiken MF, Wang F, Price CM. 2012. Maintaining the end: Roles of telomere proteins in end-protection, telomere replication and length regulation. Mutat Res 730: 12-19.
128. Stone MS, Mihalusova M, O'Connor CM, Prathapam R, Collins K, Zhuang X. 2007. Stepwise protein-mediated RNA folding directs assembly of telomerase ribonucleoprotein. Nature 446: 458-461.
129. Taggart AK, Teng SC, Zakian VA. 2002. Est1p as a cell cycle-regulated activator of telomere-bound telomerase. Science 297: 1023-1026.
130. Talley JM, DeZwaan DC, Maness LD, Freeman BC, Friedman KL. 2011. Stimulation of yeast telomerase activity by the ever shorter telomere 3 (Est3) subunit is dependent on direct interaction with the catalytic protein Est2. J Biol Chem 286: 26431-26439.
131. Tang W, Kannan R, Blanchette M, Baumann P. 2012. Telomerase RNA biogenesis involves sequential binding by Sm and Lsm complexes. Nature 484: 260-264.
132. Teixeira MT, Gilson E. 2005. Telomere maintenance, function and evolution: The yeast paradigm. Chromosome Res 13: 535-548.
133. Teixeira MT, Forstemann K, Gasser SM, Lingner J. 2002. Intracellular trafficking of yeast telomerase components. EMBO Rep 3: 652-659.
134. Tejera AM, Stagno d'Alcontres M, Thanasoula M, Marion RM, Martinez P, Liao C, Flores JM, Tarsounas M, Blasco MA. 2010. TPP1 is required for TERT recruitment, telomere elongation during nuclear reprogramming, and normal skin development in mice. Dev Cell 18: 775-789.
135. Theimer CA, Feigon J. 2006. Structure and function of telomerase RNA. Curr Opin Struct Biol 16: 307-318.
136. Theimer CA, Jády BE, Chim N, Richard P, Breece KE, Kiss T, Feigon J. 2007. Structural and functional characterization of human telomerase RNA processing and Cajal body localization signals. Mol Cell 27: 869-881.
137. Ting NS, Yu Y, Pohorelic B, Lees-Miller SP, Beattie TL. 2005. Human Ku70/80 interacts directly with hTR, the RNA component of human telomerase. Nucleic Acids Res 33: 2090-2098.
138. Tomita K, Cooper JP. 2008. Fission yeast Ccq1 is telomerase recruiter and local checkpoint controller. Genes Dev 22: 3461-3474.
139. Tomlinson RL, Ziegler TD, Supakorndej T, Terns RM, Terns MP. 2006. Cell cycle-regulated trafficking of human telomerase to telomeres. Mol Biol Cell 17: 955-965.
140. Tomlinson RL, Abreu EB, Ziegler T, Ly H, Counter CM, Terns RM, Terns MP. 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.
141. Tuzon CT, Wu Y, Chan A, Zakian VA. 2011. The Saccharomyces cerevisiae telomerase subunit Est3 binds telomeres in a cell cycleand Est1-dependent manner and interacts directly with Est1 in vitro. PLoS Genet 7: e1002060. doi: 10.1371/journal.pgen.1002060.
142. Tycowski KT, 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.
143. Tzfati Y, Fulton TB, Roy J, Blackburn EH. 2000. Template boundary in a yeast telomerase specified by RNA structure. Science 288: 863-867.
144. Tzfati Y, Knight Z, Roy J, Blackburn EH. 2003. A novel pseudoknot element is essential for the action of a yeast telomerase. Genes Dev 17: 1779-1788.
145. Venteicher AS, Meng Z, Mason PJ, Veenstra TD, Artandi SE. 2008. Identification of ATPases pontin and reptin as telomerase components essential for holoenzyme assembly. Cell 132: 945-957.
146. Venteicher AS, Abreu EB, Meng Z, McCann KE, Terns RM, Veenstra TD, Terns MP, Artandi SE. 2009. A human telomerase holoenzyme protein required for Cajal body localization and telomere synthesis. Science 323: 644-648.
147. Walbott H, Machado-Pinilla R, Liger D, Blaud M, Rety S, Grozdanov PN, Godin K, van Tilbeurgh H, Varani G, Meier UT, et al. 2011. The H/ACA RNP assembly factor SHQ1 functions as an RNA mimic. Genes Dev 25: 2398-2408.
148. Wang C, Meier UT. 2004. Architecture and assembly of mammalian H/ACA small nucleolar and telomerase ribonucleoproteins. EMBO J 23: 1857-1867.
149. 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.
150. Wang Y, Ghosh G, Hendrickson EA. 2009. Ku86 represses lethal telomere deletion events in human somatic cells. Proc Natl Acad Sci 106: 12430-12435.
151. Watson JM, Riha K. 2010. Comparative biology of telomeres: Where plants stand. FEBS Lett 584: 3752-3759.
152. Webb CJ, 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.
153. Weinrich SL, Pruzan R, Ma L, Ouellette M, Tesmer VM, Holt SE, Bodnar AG, Lichsteiner S, Kim NW, Trager JB, et al. 1997. Reconstitution of human telomerase with the template RNA component hTR and the catalytic protein subunit hTRT. Nat Genet 17: 498-502.
154. Witkin KL, Collins K. 2004. Holoenzyme proteins required for the physiological assembly and activity of telomerase. Genes Dev 18: 1107-1118.
155. Witkin KL, Prathapam R, Collins K. 2007. Positive and negative regulation of Tetrahymena telomerase holoenzyme. Mol Cell Biol 27: 2074-2083.
156. Wu Y, Zakian VA. 2011. The telomeric Cdc13 protein interacts directly with the telomerase subunit Est1 to bring it to telomeric DNA ends in vitro. Proc Natl Acad Sci 108: 20362-20369.
157. Wyatt HD, West SC, Beattie TL. 2010. InTERTpreting telomerase structure and function. Nucleic Acids Res 38: 5609-5622.
158. Xie M, Podlevsky JD, Qi X, Bley CJ, Chen JJ. 2010. A novel motif in telomerase reverse transcriptase regulates telomere repeat addition rate and processivity. Nucleic Acids Res 38: 1982-1996.
159. 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-β and interacts with POT1 to recruit telomerase. Nature 445: 559-562.
160. ATM and Rad3ATR phosphorylate the telomere protein Ccq1 to recruit telomerase and elongate telomeres in fission yeast. Genes Dev 26: 241-246.
161. Yang Y, Isaac C, Wang C, Dragon F, Pogacic V, Meier UT. 2000. Conserved composition of mammalian box H/ACA and box C/D small nucleolar ribonucleoprotein particles and their interaction with the common factor Nopp140. Mol Biol Cell 11: 567-577.
162. Yen WF, Chico L, Lei M, Lue NF. 2011. Telomerase regulatory subunit Est3 in two Candida species physically interacts with the TEN domain of TERT and telomeric DNA. Proc Natl Acad Sci 108: 20370-20375.
163. Yi X, Tesmer VM, Savre-Train I, Shay JW, Wright WE. 1999. Both transcriptional and posttranscriptional mechanisms regulate human telomerase template RNA levels. Mol Cell Biol 19: 3989-3997.
164. Yu EY. 2012. Telomeres and telomerase in Candida albicans. Mycoses 55: e48-e59.
165. Zappulla DC, Cech TR. 2006. RNA as a flexible scaffold for proteins: Yeast telomerase and beyond. Cold Spring Harb Symp Quant Biol 71: 217-224.
166. Zappulla DC, Goodrich K, Cech TR. 2005. A miniature yeast telomerase RNA functions in vivo and reconstitutes activity in vitro. Nat Struct Mol Biol 12: 1072-1077.
167. Zaug AJ, Podell ER, Nandakumar J, Cech TR. 2010. Functional interaction between telomere protein TPP1 and telomerase. Genes Dev 24: 613-622.
168. Zeng Z, Min B, Huang J, Hong K, Yang Y, Collins K, Lei M. 2011. Structural basis for Tetrahymena telomerase processivity factor Teb1 binding to single-stranded telomeric-repeat DNA. Proc Natl Acad Sci 108: 20357-20361.
169. Zhang Q, Kim NK, Feigon J. 2011. Architecture of human telomerase RNA. Proc Natl Acad Sci 108: 20325-20332.
170. Zhao Y, Abreu E, Kim J, Stadler G, Eskiocak U, Terns MP, Terns RM, Shay JW, Wright WE. 2011. Processive and distributive extension of human telomeres by telomerase under homeostatic and non-equilibrium conditions. Mol Cell 42: 297-307.
171. Zhong F, Savage SA, Shkreli M, Giri N, Jessop L, Myers T, Chen R, Alter BP, Artandi SE. 2011. Disruption of telomerase trafficking by TCAB1 mutation causes dyskeratosis congenita. Genes Dev 25: 11-16.