Structural basis for protein-RNA recognition in telomerase

Nature Structural and Molecular Biology

Volumn 21, Issue 6, 2014, Pages 507-512

  Huang, Jing ^a,b   Brown, Andrew F ^c   Wu, Jian ^a   Xue, Jing ^a   Bley, Christopher J ^c   Rand, Dustin P ^c   Wu, Lijie ^a   Zhang, Rongguang ^a   Chen, Julian J L ^c   Lei, Ming ^a,b  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA; TELOMERASE;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA PROTEIN COMPLEX; EUKARYOTE; MOLECULAR RECOGNITION; MUTANT; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; ORYZIAS LATIPES; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RNA CONFORMATION; RNA STRUCTURE; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS; TETRAHYMENA; WILD TYPE;

EUKARYOTA; ORYZIAS LATIPES; TELEOSTEI; TETRAHYMENA; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; ORYZIAS; PROTEIN STRUCTURE, TERTIARY; RNA; SEQUENCE HOMOLOGY; TELOMERASE;

EID: 84901985293     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2819     Document Type: Article

References (38)

1. Cech, T.R. Beginning to understand the end of the chromosome. Cell 116, 273-279 (2004). (Pubitemid 38167317)
2. Blasco, M.A. Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 6, 611-622 (2005). (Pubitemid 41044298)
3. Shay, J.W. & Wright, W.E. Telomerase therapeutics for cancer: challenges and new directions. Nat. Rev. Drug Discov. 5, 577-584 (2006). (Pubitemid 43971192)
4. Harley, C.B. Telomerase and cancer therapeutics. Nat. Rev. Cancer 8, 167-179 (2008). (Pubitemid 351305939)
5. Autexier, C. & Lue, N.F. The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 75, 493-517 (2006). (Pubitemid 44118041)
6. Gillis, A.J., Schuller, A.P. & Skordalakes, E. Structure of the Tribolium castaneum telomerase catalytic subunit TERT. Nature 455, 633-637 (2008).
7. Mitchell, M., Gillis, A., Futahashi, M., Fujiwara, H. & Skordalakes, E. Structural basis for telomerase catalytic subunit TERT binding to RNA template and telomeric DNA. Nat. Struct. Mol. Biol. 17, 513-518 (2010).
8. Chen, J.L., Blasco, M.A. & Greider, C.W. Secondary structure of vertebrate telomerase RNA. Cell 100, 503-514 (2000).
9. Chen, J.L. & Greider, C.W. Telomerase RNA structure and function: implications for dyskeratosis congenita. Trends Biochem. Sci. 29, 183-192 (2004). (Pubitemid 38472023)
10. Mitchell, J.R. & Collins, K. Human telomerase activation requires two independent interactions between telomerase RNA and telomerase reverse transcriptase. Mol. Cell 6, 361-371 (2000).
11. Mitchell, J.R., Cheng, J. & Collins, K. A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 3′ end. Mol. Cell. Biol. 19, 567-576 (1999). (Pubitemid 29018458)
12. Tesmer, V.M. et al. 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 (1999). (Pubitemid 29399325)
13. Vulliamy, T. et al. The RNA component of telomerase is mutated in autosomal dominant dyskeratosis congenita. Nature 413, 432-435 (2001). (Pubitemid 32928599)
14. Vulliamy, T., Marrone, A., Dokal, I. & Mason, P.J. Association between aplastic anaemia and mutations in telomerase RNA. Lancet 359, 2168-2170 (2002). (Pubitemid 34694028)
15. Robart, A.R. & Collins, K. Human telomerase domain interactions capture DNA for TEN domain-dependent processive elongation. Mol. Cell 42, 308-318 (2011).
16. Chen, J.L., Opperman, K.K. & Greider, C.W. A critical stem-loop structure in the CR4-CR5 domain of mammalian telomerase RNA. Nucleic Acids Res. 30, 592-597 (2002). (Pubitemid 34679622)
17. Brown, Y. et al. A critical three-way junction is conserved in budding yeast and vertebrate telomerase RNAs. Nucleic Acids Res. 35, 6280-6289 (2007). (Pubitemid 350018589)
18. Mason, D.X., Goneska, E. & Greider, C.W. Stem-loop IV of tetrahymena telomerase RNA stimulates processivity in trans. Mol. Cell. Biol. 23, 5606-5613 (2003). (Pubitemid 36951326)
19. Richards, R.J. et al. Structural study of elements of Tetrahymena telomerase RNA stem-loop IV domain important for function. RNA 12, 1475-1485 (2006). (Pubitemid 44141527)
20. Bley, C.J. et al. RNA-protein binding interface in the telomerase ribonucleoprotein. Proc. Natl. Acad. Sci. USA 108, 20333-20338 (2011).
21. Harkisheimer, M., Mason, M., Shuvaeva, E. & Skordalakes, E. A motif in the vertebrate telomerase N-terminal linker of TERT contributes to RNA binding and telomerase activity and processivity. Structure 21, 1870-1878 (2013).
22. Kim, N.K., Theimer, C.A., Mitchell, J.R., Collins, K. & Feigon, J. 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 (2010).
23. Leeper, T., Leulliot, N. & Varani, G. The solution structure of an essential stem-loop of human telomerase RNA. Nucleic Acids Res. 31, 2614-2621 (2003). (Pubitemid 37441746)
24. Kim, N.K., Zhang, Q. & Feigon, J. Structure and sequence elements of the CR4/5 domain of medaka telomerase RNA important for telomerase function. Nucleic Acids Res. 42, 3395-3408 (2013).
25. Xie, M. et al. Structure and function of the smallest vertebrate telomerase RNA from teleost fish. J. Biol. Chem. 283, 2049-2059 (2008).
26. Podlevsky, J.D., Bley, C.J., Omana, R.V., Qi, X. & Chen, J.J. The telomerase database. Nucleic Acids Res. 36, D339-D343 (2008). (Pubitemid 351149746)
27. Jiang, J. et al. The architecture of Tetrahymena telomerase holoenzyme. Nature 496, 187-192 (2013).
28. Zhang, Q., Kim, N.K., Peterson, R.D., Wang, Z. & Feigon, J. Structurally conserved five nucleotide bulge determines the overall topology of the core domain of human telomerase RNA. Proc. Natl. Acad. Sci. USA 107, 18761-18768 (2010).
29. Cash, D.D. et al. Pyrimidine motif triple helix in the Kluyveromyces lactis telomerase RNA pseudoknot is essential for function in vivo. Proc. Natl. Acad. Sci. USA 110, 10970-10975 (2013).
30. Theimer, C.A., Blois, C.A. & Feigon, J. Structure of the human telomerase RNA pseudoknot reveals conserved tertiary interactions essential for function. Mol. Cell 17, 671-682 (2005). (Pubitemid 40320917)
31. Qiao, F. & Cech, T.R. Triple-helix structure in telomerase RNA contributes to catalysis. Nat. Struct. Mol. Biol. 15, 634-640 (2008). (Pubitemid 351799131)
32. Qiao, F., Goodrich, K.J. & Cech, T.R. Engineering cis-telomerase RNAs that add telomeric repeats to themselves. Proc. Natl. Acad. Sci. USA 107, 4914-4918 (2010).
33. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
34. De La Fortelle, E. & Bricogne, G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472-494 (1997). (Pubitemid 27085618)
35. Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
36. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
37. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007). (Pubitemid 47080256)
38. Qi, X. et al. The common ancestral core of vertebrate and fungal telomerase RNAs. Nucleic Acids Res. 41, 450-462 (2013).