Structurally conserved five nucleotide bulge determines the overall topology of the core domain of human telomerase RNA

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 44, 2010, Pages 18761-18768

  Zhang, Qi ^a   Kim, Nak Kyoon ^a   Peterson, Robert D ^a   Wang, Zhonghua ^a   Feigon, Juli ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

REPETITIVE DNA; TELOMERASE;

3' UNTRANSLATED REGION; AMINO ACID SEQUENCE; CATALYSIS; CHROMOSOME; CONFERENCE PAPER; CONTROLLED STUDY; DNA TEMPLATE; ENZYME ACTIVITY; ENZYME STRUCTURE; HEPATITIS C; HUMAN; INTERNAL RIBOSOME ENTRY SITE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; RNA STRUCTURE;

HEPATITIS C VIRUS; VERTEBRATA;

EID: 78650452333     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1013269107     Document Type: Article

References (63)

1. Palm W, de Lange T (2008) How shelterin protects mammalian telomeres. Annu Rev Genet 42:301-334.
2. Greider CW, Blackburn EH (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43:405-413.
3. Cech TR (2004) Beginning to understand the end of the chromosome. Cell 116:273-279.
4. 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.
5. Blasco MA (2005) Telomeres and human disease: Ageing, cancer and beyond. Nat Rev Genet 6:611-622.
6. Greider CW, Blackburn EH (1989) A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337:331-337.
7. Collins K (2006) The biogenesis and regulation of telomerase holoenzymes. Nat Rev Mol Cell Biol 7:484-494.
8. Chen JL, Blasco MA, Greider CW (2000) Secondary structure of vertebrate telomerase RNA. Cell 100:503-514.
9. Theimer CA, Feigon J (2006) Structure and function of telomerase RNA. Curr Opin Struct Biol 16:307-318.
10. Collins K (2008) Physiological assembly and activity of human telomerase complexes. Mech Ageing Dev 129:91-98.
11. Armanios M (2009) Syndromes of telomere shortening. Annu Rev Genom Hum G 10:45-61.
12. 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.
13. Autexier C, Pruzan R, Funk WD, Greider CW (1996) Reconstitution of human telomerase activity and identification of a minimal functional region of the human telomerase RNA. EMBO J 15:5928-5935.
14. Mitchell JR, Collins K (2000) Human telomerase activation requires two independent interactions between telomerase RNA and telomerase reverse transcriptase. Mol Cell 6:361-371.
15. Podlevsky JD, Bley CJ, Omana RV, Qi X, Chen JJ (2008) The telomerase database. Nucleic Acids Res 36:D339-343.
16. Lin J, et al. (2004) A universal telomerase RNA core structure includes structured motifs required for binding the telomerase reverse transcriptase protein. Proc Natl Acad Sci USA 101:14713-14718.
17. Chen JL, Greider CW (2004) An emerging consensus for telomerase RNA structure. Proc Natl Acad Sci USA 101:14683-14684.
18. 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.
19. Autexier C, Lue NF (2006) The structure and function of telomerase reverse transcriptase. Annu Rev Biochem 75:493-517.
20. 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.
21. Gillis AJ, Schuller AP, Skordalakes E (2008) Structure of the Tribolium castaneum telomerase catalytic subunit TERT. Nature 455:633-637.
22. 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.
23. 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.
24. Kim NK, et al. (2008) Solution structure and dynamics of the wild-type pseudoknot of human telomerase RNA. J Mol Biol 384:1249-1261.
25. Shefer K, et al. (2007) A triple helix within a pseudoknot is a conserved and essential element of telomerase RNA. Mol Cell Biol 27:2130-2143.
26. Qiao F, Cech TR (2008) Triple-helix structure in telomerase RNA contributes to catalysis. Nat Struct Mol Biol 15:634-640.
27. Xie M, et al. (2008) Structure and function of the smallest vertebrate telomerase RNA from teleost fish. J Biol Chem 283:2049-2059.
28. Chen JL, Greider CW(2003) Determinants in mammalian telomerase RNA that mediate enzyme processivity and cross-species incompatibility. EMBO J 22:304-314.
29. Gavory G, Symmons MF, Krishnan Ghosh Y, Klenerman D, Balasubramanian S (2006) Structural analysis of the catalytic core of human telomerase RNA by FRET and molecular modeling. Biochemistry 45:13304-13311.
30. Comolli LR, Smirnov I, Xu L, Blackburn EH, James TL (2002) A molecular switch underlies a human telomerase disease. Proc Natl Acad Sci USA 99:16998-17003.
31. Theimer CA, Finger LD, Trantirek L, Feigon J (2003) Mutations linked to dyskeratosis congenita cause changes in the structural equilibrium in telomerase RNA. Proc Natl Acad Sci USA 100:449-454.
32. Chen JL, Greider CW (2005) Functional analysis of the pseudoknot structure in human telomerase RNA. Proc Natl Acad Sci USA 102:8080-8085.
33. Prestegard JH, Al-Hashimi HM, Tolman JR (2000) NMR structures of biomolecules using field oriented media and residual dipolar couplings. Q Rev Biophys 33:371-424.
34. Zhang Q, Sun X, Watt ED, Al-Hashimi HM (2006) Resolving the motional modes that code for RNA adaptation. Science 311:653-656.
35. Lipari G, Szabo A (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J Am Chem Soc 104:4546-4559.
36. Clore GM, et al. (1990) Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J Am Chem Soc 112:4989-4991.
37. Mandel AM, Akke M, Palmer AG, 3rd (1995) Backbone dynamics of Escherichia coli ribonuclease HI: Correlations with structure and function in an active enzyme. J Mol Biol 246:144-163.
38. Palmer AG, 3rd (2004) NMR characterization of the dynamics of biomacromolecules. Chem Rev 104:3623-3640.
39. Tjandra N, Bax A (1997) Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278:1111-1114.
40. Getz M, Sun X, Casiano-Negroni A, Zhang Q, Al-Hashimi HM (2007) NMR studies of RNA dynamics and structural plasticity using NMR residual dipolar couplings. Biopolymers 86:384-402.
41. Zhang Q, Stelzer AC, Fisher CK, Al-Hashimi HM (2007) Visualizing spatially correlated dynamics that directs RNA conformational transitions. Nature 450:1263-1267.
42. Bailor MH, Sun X, Al-Hashimi HM (2010) Topology links RNA secondary structure with global conformation, dynamics, and adaptation. Science 327:202-206.
43. Huard S, Moriarty TJ, Autexier C (2003) The C terminus of the human telomerase reverse transcriptase is a determinant of enzyme processivity. Nucleic Acids Res 31:4059-4070.
44. Parisien M, Major F (2008) The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data. Nature 452:51-55.
45. Chen JL, Greider CW (2004) Telomerase RNA structure and function: Implications for dyskeratosis congenita. Trends Biochem Sci 29:183-192.
46. Antal M, Boros E, Solymosy F, Kiss T (2002) Analysis of the structure of human telomerase RNA in vivo. Nucleic Acids Res 30:912-920.
47. Qiao F, Goodrich KJ, Cech TR (2010) Engineering cis-telomerase RNAs that add telomeric repeats to themselves. Proc Natl Acad Sci USA 107:4914-4918.
48. Popenda M, et al. (2010) RNA FRABASE 2.0: An advanced web-accessible database with the capacity to search the three-dimensional fragments within RNA structures. BMC Bioinformatics 11:231.
49. Lukavsky PJ, Kim I, Otto GA, Puglisi JD (2003) Structure of HCV IRES domain II determined by NMR. Nat Struct Biol 10:1033-1038.
50. Locker N, Easton LE, Lukavsky PJ (2007) HCV and CSFV IRES domain II mediate eIF2 release during 80S ribosome assembly. EMBO J 26:795-805.
51. Parsons J, et al. (2009) Conformational inhibition of the hepatitis C virus internal ribosome entry site RNA. Nat Chem Biol 5:823-825.
52. Paulsen RB, et al. (2010) Inhibitor-induced structural change in the HCV IRES domain IIa RNA. Proc Natl Acad Sci USA 107:7263-7268.
53. Dieckmann T, Feigon J (1997) Assignment methodology for larger RNA oligonucleotides: Application to an ATP-binding RNA aptamer. J Biomol NMR 9:259-272.
54. Peterson RD, Theimer CA, Wu H, Feigon J (2004) New applications of 2D filtered/edited NOESY for assignment and structure elucidation of RNA and RNA-protein complexes. J Biomol NMR 28:59-67.
55. Clore GM, et al. (1990) Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J Am Chem Soc 112:4989-4991.
56. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160:65-73.
57. Wu H, et al. (2001) A novel family of RNA tetraloop structure forms the recognition site for Saccharomyces cerevisiae RNase III. EMBO J 20:7240-7249.
58. Case DA, et al. (2002) AMBER 7 (University of California, San Francisco).
59. Stefl R, Wu H, Ravindranathan S, Sklenar V, Feigon J (2004) DNA A-tract bending in three dimensions: Solving the dA4T4 vs. dT4A4 conundrum. Proc Natl Acad Sci USA 101:1177-1182.
60. Wang JM, Cieplak P, Kollman PA (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J Comput Chem 21:1049-1074.
61. Bailor MH, et al. (2007) Characterizing the relative orientation and dynamics of RNA A-form helices using NMR residual dipolar couplings. Nat Protoc 2:1536-1546.
62. Kim NK, Theimer CA, Mitchell JR, Collins K, Feigon J (2010) Effect of pseudouridylation on the structure and activity of the catalytically essential P6.1 hairpin in human telomerase RNA. Nucleic Acids Res 10.1093/nar/gkq525.
63. Wang F, et al. (2007) The POT1-TPP1 telomere complex is a telomerase processivity factor. Nature 445:506-510.