Human telomerase specialization for repeat synthesis by unique handling of primer-template duplex

EMBO Journal

Volumn 33, Issue 8, 2014, Pages 921-935

  Wu, Robert Alexander ^a   Collins, Kathleen ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

primer template hybrid; reverse transcriptase; single stranded DNA; telomerase RNP; telomeric repeats

Indexed keywords

RNA; SINGLE STRANDED DNA; TELOMERASE REVERSE TRANSCRIPTASE;

ARTICLE; CONTROLLED STUDY; DNA RNA HYBRIDIZATION; DNA TEMPLATE; ENZYME ACTIVE SITE; ENZYME SYNTHESIS; GENE REPLICATION; HUMAN; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN FOOTPRINTING;

DNA; HUMANS; REPETITIVE SEQUENCES, NUCLEIC ACID; RNA; TELOMERASE; TEMPLATES, GENETIC;

EID: 84898880765     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1002/embj.201387205     Document Type: Article

References (60)

1. Alder JK, Cogan JD, Brown AF, Anderson CJ, Lawson WE, Lansdorp PM, Phillips JA 3rd, Loyd JE, Chen JJ, Armanios M, (2011) Ancestral mutation in telomerase causes defects in repeat addition processivity and manifests as familial pulmonary fibrosis. PLoS Genet 7: e1001352
2. Armanios M, Blackburn EH, (2012) The telomere syndromes. Nat Rev Genet 13: 693-704
3. Bairley RC, Guillaume G, Vega LR, Friedman KL, (2011) A mutation in the catalytic subunit of yeast telomerase alters primer-template alignment while promoting processivity and protein-DNA binding. J Cell Sci 124: 4241-4252
4. Berman AJ, Akiyama BM, Stone MD, Cech TR, (2011) The RNA accordion model for template positioning by telomerase RNA during telomeric DNA synthesis. Nat Struct Mol Biol 18: 1371-1375
5. Blackburn EH, Collins K, (2011) Telomerase: an RNP enzyme synthesizes DNA. Cold Spring Harb Perspect Biol 3: a003558
6. 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
7. 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
8. Chase JW, Richardson CC, (1974) Exonuclease VII of Escherichia coli. Mechanism of action. J Biol Chem 249: 4553-4561
9. Chen JL, Blasco MA, Greider CW, (2000) Secondary structure of vertebrate telomerase RNA. Cell 100: 503-514
10. Chen JL, Greider CW, (2003) Template boundary definition in mammalian telomerase. Genes Dev 17: 2747-2752
11. Chen JL, Greider CW, (2005) Functional analysis of the pseudoknot structure in human telomerase RNA. Proc Natl Acad Sci USA 102: 8080-8085
12. Collins K, (2011) Single-stranded DNA repeat synthesis by telomerase. Curr Opin Chem Biol 15: 643-648
13. Collins K, Greider CW, (1993) Tetrahymena telomerase catalyzes nucleolytic cleavage and nonprocessive elongation. Genes Dev 7: 1364-1376
14. Das R, Laederach A, Pearlman SM, Herschlag D, Altman RB, (2005) SAFA: semi-automated footprinting analysis software for high-throughput quantification of nucleic acid footprinting experiments. RNA 11: 344-354
15. Drosopoulos WC, Direnzo R, Prasad VR, (2005) Human telomerase RNA template sequence is a determinant of telomere repeat extension rate. J Biol Chem 280: 32801-32810
16. 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
17. Egan ED, Collins K, (2012) Biogenesis of telomerase ribonucleoproteins. RNA 18: 1747-1759
18. Finger SN, Bryan TM, (2008) Multiple DNA-binding sites in Tetrahymena telomerase. Nucleic Acids Res 36: 1260-1272
19. Förstemann K, Lingner J, (2005) Telomerase limits the extent of base pairing between template RNA and telomeric DNA. EMBO Rep 6: 361-366
20. Fu D, Collins K, (2003) Distinct biogenesis pathways for human telomerase RNA and H/ACA small nucleolar RNAs. Mol Cell 11: 1361-1372
21. Gillis AJ, Schuller AP, Skordalakes E, (2008) Structure of the Tribolium castaneum telomerase catalytic subunit TERT. Nature 455: 633-637
22. 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
23. Jiang J, Miracco EJ, Hong K, Eckert B, Chan H, Cash DD, Min B, Zhou ZH, Collins K, Feigon J, (2013) The architecture of Tetrahymena telomerase holoenzyme. Nature 496: 187-192
24. Jurczyluk J, Nouwens AS, Holien JK, Adams TE, Lovrecz GO, Parker MW, Cohen SB, Bryan TM, (2010) Direct involvement of the TEN domain at the active site of human telomerase. Nucleic Acids Res 39: 1774-1788
25. Lai CK, Miller MC, Collins K, (2002) Template boundary definition in Tetrahymena telomerase. Genes Dev 16: 415-420
26. Lee MS, Blackburn EH, (1993) Sequence-specific DNA primer effects on telomerase polymerization activity. Mol Cell Biol 13: 6586-6599
27. Lewis KA, Wuttke DS, (2012) Telomerase and telomere-associated proteins: structural insights into mechanism and evolution. Structure 20: 28-39
28. Lue NF, (2005) A physical and functional constituent of telomerase anchor site. J Biol Chem 280: 26586-26591
29. Ly H, Blackburn EH, Parslow TG, (2003) Comprehensive structure-function analysis of the core domain of human telomerase RNA. Mol Cell Biol 23: 6849-6856
30. Miller MC, Collins K, (2002) Telomerase recognizes its template by using an adjacent RNA motif. Proc Natl Acad Sci USA 99: 6585-6590
31. 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
32. 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
33. Moriarty TJ, Marie-Egyptienne DT, Autexier C, (2004) Functional organization of repeat addition processivity and DNA synthesis determinants in the human telomerase multimer. Mol Cell Biol 24: 3720-3733
34. Moriarty TJ, Marie-Egyptienne DT, Autexier C, (2005) Regulation of 5′ template usage and incorporation of noncognate nucleotides by human telomerase. RNA 11: 1448-1460
35. Morin GB, (1989) The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell 59: 521-529
36. Morin GB, (1991) Recognition of a chromosome truncation site associated with alpha-thalassaemia by human telomerase. Nature 353: 454-456
37. Nandakumar J, Cech TR, (2013) Finding the end: recruitment of telomerase to telomeres. Nat Rev Mol Cell Biol 14: 69-82
38. 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
39. Oganesian L, Moon IK, Bryan TM, Jarstfer MB, (2006) Extension of G-quadruplex DNA by ciliate telomerase. EMBO J 25: 1148-1159
40. Pascolo E, Wenz C, Lingner J, Hauel N, Priepke H, Kauffmann I, Garin-Chesa P, Rettig WJ, Damm K, Schnapp A, (2002) Mechanism of human telomerase inhibition by BIBR1532, a synthetic, non-nucleosidic drug candidate. J Biol Chem 277: 15566-15572
41. Podlevsky JD, Bley CJ, Omana RV, Qi X, Chen JJ, (2008) The telomerase database. Nucleic Acids Res 36: D339-D343
42. Podlevsky JD, Chen JJ, (2012) It all comes together at the ends: telomerase structure, function, and biogenesis. Mutat Res 730: 3-11
43. Qi X, Li Y, Honda S, Hoffmann S, Marz M, Mosig A, Podlevsky JD, Stadler PF, Selker EU, Chen JJ, (2013) The common ancestral core of vertebrate and fungal telomerase RNAs. Nucleic Acids Res 41: 450-462
44. 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
45. Qiao F, Cech TR, (2008) Triple-helix structure in telomerase RNA contributes to catalysis. Nat Struct Mol Biol 15: 634-640
46. 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
47. Robart AR, Collins K, (2011) Human telomerase domain interactions capture DNA for TEN domain-dependent processive elongation. Mol Cell 42: 308-318
48. Romi E, Baran N, Gantman M, Shmoish M, Min B, Collins K, Manor H, (2007) High-resolution physical and functional mapping of the template adjacent DNA binding site in catalytically active telomerase. Proc Natl Acad Sci USA 104: 8791-8796
49. Sealey DC, Zheng L, Taboski MA, Cruickshank J, Ikura M, Harrington LA, (2010) The N-terminus of hTERT contains a DNA-binding domain and is required for telomerase activity and cellular immortalization. Nucleic Acids Res 38: 2019-2035
50. Shay JW, Wright WE, (2011) Role of telomeres and telomerase in cancer. Sem Cancer Biol 21: 349-353
51. Theimer CA, Blois CA, Feigon J, (2005) Structure of the human telomerase RNA pseudoknot reveals conserved tertiary interactions essential for function. Mol Cell 17: 671-682
52. Tzfati Y, Fulton TB, Roy J, Blackburn EH, (2000) Template boundary in a yeast telomerase specified by RNA structure. Science 288: 863-867
53. Wallweber G, Gryaznov S, Pongracz K, Pruzan R, (2003) Interaction of human telomerase with its primer substrate. Biochemistry 42: 589-600
54. Weinrich SL, Pruzan R, Ma L, Ouellette M, Tesmer VM, Holt SE, Bodnar AG, Lichtsteiner S, Kim NW, Trager JB, Taylor RD, Carlos R, Andrews WH, Wright WE, Shay JW, Harley CB, Morin GB, (1997) Reconstitution of human telomerase with the template RNA component hTR and the catalytic protein subunit hTRT. Nat Genet 17: 498-502
55. Wyatt HD, Lobb DA, Beattie TL, (2007) Characterization of physical and functional anchor site interactions in human telomerase. Mol Cell Biol 27: 3226-3240
56. Wyatt HD, West SC, Beattie TL, (2010) InTERTpreting telomerase structure and function. Nucleic Acids Res 38: 5609-5622
57. Xia J, Peng Y, Mian IS, Lue NF, (2000) Identification of functionally important domains in the N-terminal region of telomerase reverse transcriptase. Mol Cell Biol 20: 5196-5207
58. Zaug AJ, Podell ER, Cech TR, (2008) Mutation in TERT separates processivity from anchor-site function. Nat Struct Mol Biol 15: 870-872
59. Zhang Q, Kim NK, Feigon J, (2011) Architecture of human telomerase RNA. Proc Natl Acad Sci USA 108: 20325-20332
60. 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 nonequilibrium conditions. Mol Cell 42: 297-307