Structure of stem-loop IV of Tetrahymena telomerase RNA

EMBO Journal

Volumn 25, Issue 13, 2006, Pages 3156-3166

  Chen, Yu ^a   Fender, Jessica ^a   Legassie, Jason D ^b   Jarstfer, Michael B ^b   Bryan, Tracy M ^c   Varani, Gabriele ^a,d  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

NMR; Ribonucleoprotein; RNA structure; Stem loop; Telomerase

Indexed keywords

HOLOENZYME; RNA; TELOMERASE REVERSE TRANSCRIPTASE;

ARTICLE; BINDING AFFINITY; CATALYSIS; CHEMICAL STRUCTURE; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; REVERSE TRANSCRIPTION; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

ANIMALS; BASE SEQUENCE; DNA-BINDING PROTEINS; ENZYME ACTIVATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; RNA; RNA, PROTOZOAN; TELOMERASE; TETRAHYMENA THERMOPHILA;

CILIOPHORA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

EID: 33746298321     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601195     Document Type: Article

References (56)

1. Al-Hashimi HM, Gosser Y, Gorin A, Hu W, Majumdar A, Patel DJ (2002) Concerted motions in HIV-1 TAR RNA may allow access to bound state conformations: RNA dynamics from NMR residual dipolar couplings. J Mol Biol 315: 95-102
2. Allain FHT, Varani G (1995) Divalent metal ion binding to a conserved wobble pair defining the upstream site of cleavage of group I self-splicing introns. Nucleic Acids Res 23: 341-350
3. Andersson P, Nordstrand K, Sunnerhagen M, Liepinsh E, Turovskis I, Otting G (1998) Heteronuclear correlation experiments for the determination of one-bond coupling constants. J Biomol NMR 11: 445-450
4. Autexier C, Greider CW (1998) Mutational analysis of the Tetrahymena telomerase RNA: identification of residues affecting telomerase activity in vitro. Nucleic Acids Res 26: 787-795
5. Bhattacharyya A, Blackburn EH (1994) Architecture of telomerase RNA. EMBO J 23: 5721-5731
6. Blasco MA, Gasser SM, Lingner J (1999) Telomeres and telomerase. Genes Dev 13: 2353-2359
7. Blasco MA, Lee HW, Hande MP, Samper E, Lansdorp PM, DePinho RA, Greider CW (1997) Telomere shortening and tumor formation by mouse cells Lacking telomerase RNA. Cell 91: 25-34
8. Bryan TM, Goodrich KJ, Cech TR (2000) A mutant of Tetrahymena telomerase reverse transcriptase with increased processivity. J Biol Chem 275: 24199-24207
9. Bryan TM, Goodrich KJ, Cech TR (2003) Tetrahymena telomerase is active as a monomer. Mol Biol Cell 14: 4794-4804
10. Cate JH, Hanna RL, Doudna JA (1997) A magnesium ion core at the heart of a ribozyme domain. Nat Struct Biol 4: 553-558
11. Chen JL, Blasco MA, Greider CW (2000) Secondary Structure of vertebrate telomerase RNA. Cell 100: 503-514
12. Chen JL, Keyer Opperman K, Greider CW (2002) A critical stem-loop structure in the CR4-CR5 domain of mammalian telomerase RNA. Nucleic Acids Res 30: 592-597
13. Cruse WBT, Saludijan P, Biala E, Strazewski P, Prangé T, Kennard O (1994) Structure of a mispaired RNA double helix at 1.6 Å resolution and implications for the prediction of RNA secondary structure. Proc Natl Acad Sci USA 91: 4160-4164
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. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293
16. de Lange T, Jacks T (1999) For better or worse? Telomerase inhibition and cancer. Cell 98: 273-275
17. De Lano WL (2002) The PyMOL Molecular Graphics System. San Carlos USA: Delano Scientific
18. NN couplings. J Am Chem Soc 120: 8293-8297
19. Feng J, Funk WD, Wang SS, Weinrich SL, Avilion AA, Chiu CP, Adams RR, Chang E, Allsopp RC, Yu Y, Le S, West MD, Harley CB, Andrews WH, Greider CW, Villeponteau B (1995) The RNA component of human telomerase. Science 269: 1236-1241
20. Goddard TD, Kneller DG (2003) Sparky 3. San Francisco: University of California
21. Greatorex J, Gallego J, Varani G, Lever A (2002) Structure and stability of wild-type and mutant RNA internal loops from the SL-1 domain of the HIV-1 packaging signal. J Mol Biol 322: 543-557
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. Koradi R, Billeter M, Wüthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14: 51-55
24. Lai CK, Miller MC, Collins K (2003) Roles for RNA in telomerase nucleotide and repeat addition processivity. Mol Cell 11: 1673-1683
25. Lai CK, Mitchell JR, Collins K (2001) RNA binding domain of telomerase reverse transcriptase. Mol Cell Biol 21: 990-1000
26. Lavery R, Sklenar H (1988) The definition of generalized helicoidal parameters and of axis curvature for irregular nucleic acids. J Biomol Struct Dyn 6: 63-91
27. Lee HW, Blasco MA, Gottlieb GJ, Horner JWI, Greider CW, DePinho RA (1998) Essential role of mouse telomerase in highly proliferative organs. Nature 392: 569-574
28. Leeper T, Leulliot N, Varani G (2003) The solution structure of an essential stem-loop of human telomerase RNA. Nucleic Acids Res 31: 2614-2621
29. Leeper TC, Varani G (2005) The structure of an enzyme-activating fragment of human telomerase RNA. RNA 11: 394-403
30. Lingner J, Cech TR (1998) Telomerase and chromosome end maintenance. Curr Opin Gen Dev 8: 226-232
31. Lingner J, Hendrick LL, Cech TR (1994) Telomerase RNAs of different ciliates have a common secondary structure and a permuted template. Genes Dev 8: 1984-1998
32. Lingner J, Hughes TR, Shevchenko A, Mann M, Lundblad V, Cech TR (1997) Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276: 561-567
33. Lukavsky PJ, Kim I, Otto GA, Puglisi JD (2003) Structure of HCV IRES domain II determined by NMR. Nat Struct Biol 10: 1033-1038
34. Mason DX, Goneska E, Greider CW (2003) Stem-loop IV of Tetrahymena telomerase RNA stimulates processivity in trans. Mol Cell Biol 23: 5606-5613
35. Merino EJ, Wilkinson KA, Coughlan JL, Weeks KM (2005) RNA structure analysis at single nucleotide resolution by selective 2′-hydroxyl acylation and primer extension (SHAPE). J Am Chem Soc 127: 4223-4231
36. Mitchell JR, Cheng J, 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
37. Mitchell JR, Collins K (2000) Human telomerase action requires two independent interactions between telomerase RNA and telomerase reverse transcriptase. Mol Cell 6: 361-371
38. 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
39. 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
40. Pervushin K, Ono A, Fernandez C, Szyperski T, Kainosho M, Wüthrich K (1998) NMR scalar coupling across Watson-Crick base pair hydrogen bonds in DNA observed by transverse relaxation-optimized spectroscopy. Proc Natl Acad Sci USA 95: 14147-14151
41. Prathapam R, Witkin KL, O'Connor CM, Collins K (2005) A telomerase holoenzyme protein enhances telomerase RNA assembly with telomerase reverse transcriptase. Nat Stru Mol Biol 12: 252-257
42. Price SR, Oubridge C, Varani G, Nagai K (1998) Preparation of RNA-protein complexes for X-ray crystallography and NMR. In RNA-Protein Interaction: Practical Approach, Smith C (ed.) pp 37-74. Oxford: Oxford University Press
43. Roy J, Fulton TB, Blackburn EH (1998) Specific telomerase RNA residues distant from the template are essential for telomerase function. Genes Dev 12: 3286-3300
44. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Res 160: 65-73
45. 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
46. 13C NMR relaxation studies of RNA base and ribose nuclei reveal a complex pattern of motions in the RNA binding site for human U1A protein. J Mol Biol 349: 699-715
47. Sperger JM, Cech TR (2001) A stem-loop of Tetrahymena telomerase RNA distant from the template potentiates RNA folding and telomerase activity. Biochemistry 40: 7005-7016
48. Tesmer VM, Ford LP, Holt SE, Frank BC, Yi X, Aisner DL, Ouellette M, Shay JW, Wright WE (1999) Two inactive fragments of the integral RNA cooperate to assemble active telomerase with the human protein catalytic subunit (hTERT) in vitro. Mol Cell Biol 19: 6207-6216
49. Varani G, Aboul-ela F, Allain FHT (1996) NMR investigations of RNA structure. Progr NMR Spectr 29: 51-127
50. Wang C, Meier UT (2004) Architecture and assembly of mammalian H/ACA small nucleolar and telomerase ribonucleoproteins. EMBO J 23: 1857-1867
51. Wilkinson KA, Merino EJ, Weeks KM (2005) RNA SHAPE chemistry reveals nonhierarchical interactions dominate equilibrium structural transitions in tRNA(Asp) transcripts. J Am Chem Soc 127: 4659-4667
52. Witkin KL, Collins K (2004) Holoenzyme proteins required for the physiological assembly and activity of telomerase. Genes Dev 17: 1107-1118
53. Ye AJ, Romero DP (2002) Phylogenetic relationship amongst tetrahymenine ciliates inferred by a comparison of telomerase RNAs. Inter J System Evol Microbiol 52: 2297-2302
54. Zappulla DC, Cech TR (2004) Yeast telomerase RNA: a flexible scaffold for protein subunits. Proc Natl Acad Sci USA 101: 10024-10029
55. 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: 1272-1277
56. Zaug AJ, Cech TR (1995) Analysis of the structure of Tetrahymena nuclear RNAs in vivo: Telomerase RNA, the self-splicing rRNA intron and U2 snRNA. RNA 1: 363-374