Human telomerase reverse transcriptase binds to a pre-organized hTR in vivo exposing its template

Nucleic Acids Research

Volumn 44, Issue 1, 2016, Pages 413-425

  Zemora, Georgeta ^a   Handl, Stefan ^a   Waldsich, Christina ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TELOMERASE RNA; UNCLASSIFIED DRUG; PROTEIN BINDING; RNA; TERT PROTEIN, HUMAN;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA TEMPLATE; ENZYME BINDING; ENZYME STRUCTURE; HUMAN; HYDROGEN BOND; IN VIVO STUDY; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; STRUCTURE ACTIVITY RELATION; TELOMERE HOMEOSTASIS; CHEMISTRY; CONFORMATION; GENETICS; HEK293 CELL LINE; METABOLISM; MUTATION; RNA FOLDING; RNA STABILITY;

HEK293 CELLS; HUMANS; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; RNA; RNA FOLDING; RNA STABILITY; TELOMERASE;

EID: 84959553785     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1065     Document Type: Article

References (51)

1. Olovnikov,A.M. (1973) A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J. Theor. Biol., 41, 181-190.
2. Greider,C.W. and Blackburn,E.H. (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell, 43, 405-413.
3. 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.
4. Armanios,M. and Blackburn,E.H. (2012) The telomere syndromes. Nature Rev. Genet., 13, 693-704.
5. Greider,C.W. and Blackburn,E.H. (1987) The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell, 51, 887-898.
6. Weinrich,S.L., Pruzan,R., Ma,L., Ouellette,M., Tesmer,V.M., Holt,S.E., Bodnar,A.G., Lichtsteiner,S., Kim,N.W., Trager,J.B. et al. (1997 ) Reconstitution of human telomerase with the template RNA component hTR and the catalytic protein subunit hTRT. Nat. Genet., 17, 498-502.
7. Egan,E.D. and Collins,K. (2012) Biogenesis of telomerase ribonucleoproteins. RNA, 18, 1747-1759.
8. Chen,J.L., Blasco,M.A. and Greider,C.W. (2000) Secondary structure of vertebrate telomerase RNA. Cell, 100, 503-514.
9. Zhang,Q., Kim,N.K. and Feigon,J. (2011) Architecture of human telomerase RNA. Proc. Natl. Acad. Sci. U.S.A., 108, 20325-20332.
10. Greider,C.W. and Blackburn,E.H. (1989) A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature, 337, 331-337.
11. Jady,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.
12. Mitchell,J.R., Cheng,J. and 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.
13. Theimer,C.A. and Feigon,J. (2006) Structure and function of telomerase RNA. Curr. Opin. Struct. Biol., 16, 307-318.
14. Mitchell,J.R. and Collins,K. (2000) Human telomerase activation requires two independent interactions between telomerase RNA and telomerase reverse transcriptase. Mol. Cell, 6, 361-371.
15. Chen,J.L., Opperman,K.K. and Greider,C.W. (2002) A critical stem-loop structure in the CR4-CR5 domain of mammalian telomerase RNA. Nucleic Acids Res., 30, 592-597.
16. Chen,J.L. and Greider,C.W. (2004) Telomerase RNA structure and function: implications for dyskeratosis congenita. Trends Biochem. Sci., 29, 183-192.
17. Theimer,C.A., Blois,C.A. and Feigon,J. (2005) Structure of the human telomerase RNA pseudoknot reveals conserved tertiary interactions essential for function. Mol. Cell, 17, 671-682.
18. Kim,N.K., Zhang,Q., Zhou,J., Theimer,C.A., Peterson,R.D. and Feigon,J. (2008) Solution structure and dynamics of the wild-type pseudoknot of human telomerase RNA. J. Mol. Biol., 384, 1249-1261.
19. Zhang,Q., Kim,N.K., Peterson,R.D., Wang,Z. and Feigon,J. (2010) Structurally conserved five nucleotide bulge determines the overall topology of the core domain of human telomerase RNA. Proc. Natl. Acad. Sci. U.S.A., 107, 18761-18768.
20. Leeper,T., Leulliot,N. and Varani,G. (2003) The solution structure of an essential stem-loop of human telomerase RNA. Nucleic Acids Res., 31, 2614-2621.
21. Leeper,T.C. and Varani,G. (2005) The structure of an enzyme-activating fragment of human telomerase RNA. RNA, 11, 394-403.
22. Kim,N.K., Theimer,C.A., Mitchell,J.R., Collins,K. and 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., 38, 6746-6756.
23. Theimer,C.A., Jady,B.E., Chim,N., Richard,P., Breece,K.E., Kiss,T. and Feigon,J. (2007) Structural and functional characterization of human telomerase RNA processing and cajal body localization signals. Mol. Cell, 27, 869-881.
24. Qiao,F. and Cech,T.R. (2008) Triple-helix structure in telomerase RNA contributes to catalysis. Nat. Struct. Mol. Biol., 15, 634-640.
25. Kim,N.K., Zhang,Q. and Feigon,J. (2014) Structure and sequence elements of the CR4/5 domain of medaka telomerase RNA important for telomerase function. Nucleic Acids Res., 42, 3395-3408.
26. Huang,J., Brown,A.F., Wu,J., Xue,J., Bley,C.J., Rand,D.P., Wu,L., Zhang,R., Chen,J.J. and Lei,M. (2014) Structural basis for protein-RNA recognition in telomerase. Nat. Struct. Mol. Biol., 21, 507-512.
27. Cristofari,G. and Lingner,J. (2006) Telomere length homeostasis requires that telomerase levels are limiting. EMBO J., 25, 565-574.
28. Li,C., Wen,A., Shen,B., Lu,J., Huang,Y. and Chang,Y. (2011) FastCloning: a highly simplified, purification-free, sequence- and ligation-independent PCR cloning method. BMC Biotechnol., 11, 92.
29. Wildauer,M., Zemora,G., Liebeg,A., Heisig,V. and Waldsich,C. (2014) Chemical probing of RNA in living cells. Methods Mol. Biol., 1086, 159-176.
30. Waldsich,C. (2008) Dissecting RNA folding by nucleotide analog interference mapping (NAIM). Nat. Protoc., 3, 811-823.
31. Fedorova,O. and Pyle,A.M. (2005) Linking the group II intron catalytic domains: tertiary contacts and structural features of domain 3. EMBO J., 24, 3906-3916.
32. Waldsich,C. and Pyle,A.M. (2007) A folding control element for tertiary collapse of a group II intron ribozyme. Nat. Struct. Mol. Biol., 14, 37-44.
33. 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.
34. Zaug,A.J., Podell,E.R. and Cech,T.R. (2008) Mutation in TERT separates processivity from anchor-site function. Nat. Struct. Mol. Biol., 15, 870-872.
35. Ofengand,J., Del Campo,M. and Kaya,Y. (2001) Mapping pseudouridines in RNA molecules. Methods, 25, 365-373.
36. Wells,S.E., Hughes,J.M., Igel,A.H. and Ares,M. Jr (2000) Use of dimethyl sulfate to probe RNA structure in vivo. Methods Enzymol., 318, 479-493.
37. Moazed,D. and Noller,H.F. (1986) Transfer RNA shields specific nucleotides in 16S ribosomal RNA from attack by chemical probes. Cell, 47, 985-994.
38. Cash,D.D., Cohen-Zontag,O., Kim,N.K., Shefer,K., Brown,Y., Ulyanov,N.B., Tzfati,Y. and Feigon,J. (2013) Pyrimidine motif triple helix in the Kluyveromyces lactis telomerase RNA pseudoknot is essential for function in vivo. Proc. Natl. Acad. Sci. U.S.A., 110, 10970-10975.
39. Shefer,K., Brown,Y., Gorkovoy,V., Nussbaum,T., Ulyanov,N.B. and Tzfati,Y. (2007) A triple helix within a pseudoknot is a conserved and essential element of telomerase RNA. Mol. Cell. Biol., 27, 2130-2143.
40. Ly,H., Blackburn,E.H. and Parslow,T.G. (2003) Comprehensive structure-function analysis of the core domain of human telomerase RNA. Mol. Cell. Biol., 23, 6849-6856.
41. Chen,J.L. and Greider,C.W. (2003) Template boundary definition in mammalian telomerase. Genes Dev., 17, 2747-2752.
42. Brown,A.F., Podlevsky,J.D., Qi,X., Chen,Y., Xie,M. and Chen,J.J. (2014) A self-regulating template in human telomerase. Proc. Natl. Acad. Sci. U.S.A., 111, 11311-11316.
43. 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.
44. Xie,M., Mosig,A., Qi,X., Li,Y., Stadler,P.F. and Chen,J.J. (2008) Structure and function of the smallest vertebrate telomerase RNA from teleost fish. J. Biol. Chem., 283, 2049-2059.
45. Robart,A.R. and Collins,K. (2010) Investigation of human telomerase holoenzyme assembly, activity, and processivity using disease-linked subunit variants. J. Biol. Chem., 285, 4375-4386.
46. Yeoman,J.A., Orte,A., Ashbridge,B., Klenerman,D. and Balasubramanian,S. (2010) RNA conformation in catalytically active human telomerase. J. Am. Chem. Soc., 132, 2852-2853.
47. Mihalusova,M., Wu,J.Y. and Zhuang,X. (2011) Functional importance of telomerase pseudoknot revealed by single-molecule analysis. Proc. Natl. Acad. Sci. U.S.A., 108, 20339-20344.
48. Antal,M., Boros,E., Solymosy,F. and Kiss,T. (2002) Analysis of the structure of human telomerase RNA in vivo. Nucleic Acids Res., 30, 912-920.
49. Xi,L. and Cech,T.R. (2014) Inventory of telomerase components in human cells reveals multiple subpopulations of hTR and hTERT. Nucleic Acids Res., 42, 8565-8577.
50. Li,L. and Ye,K. (2006) Crystal structure of an H/ACA box ribonucleoprotein particle. Nature, 443, 302-307.
51. Egan,E.D. and Collins,K. (2010) Specificity and stoichiometry of subunit interactions in the human telomerase holoenzyme assembled in vivo. Mol. Cell. Biol., 30, 2775-2786.