Disease-associated human telomerase RNA variants show loss of function for telomere synthesis without dominant-negative interference

Molecular and Cellular Biology

Volumn 28, Issue 20, 2008, Pages 6510-6520

  Errington, Timothy M ^a,b   Fu, Dragony ^a,c   Wong, Judy M Y ^a,d   Collins, Kathleen ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c Massachusetts Institute of Technology Cambridge   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HOLOENZYME; MONOMER; RIBONUCLEOPROTEIN; RNA; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE;

APLASTIC ANEMIA; ARTICLE; CELL ASSAY; DISEASE ASSOCIATION; DYSKERATOSIS CONGENITA; ENZYME RECONSTITUTION; GENE FUNCTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SYNTHESIS; TELOMERE; WILD TYPE;

ANEMIA, APLASTIC; BASE SEQUENCE; CELL LINE; CELLS, CULTURED; CHROMATOGRAPHY, AFFINITY; DYSKERATOSIS CONGENITA; GENES, DOMINANT; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN STRUCTURE, QUATERNARY; RIBONUCLEOPROTEINS; RNA; TELOMERASE; TELOMERE; TEMPLATES, GENETIC;

EID: 53549114805     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00777-08     Document Type: Article

References (54)

1. Alves, D., H. Li, R. Codrington, A. Orte, X. Ren, D. Klenerman, and S. Balasubramanian. 2008. Single-molecule analysis of human telomerase monomer. Nat. Chem. Biol. 4:287-289.
2. Autexier, C., and N. F. Lue. 2006. The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 75:493-517.
3. Beattie, T. L., W. Zhou, M. O. Robinson, and L. Harrington. 2001. Functional multimerization of the human telomerase reverse transcriptase. Mol. Cell. Biol. 21:6151-6160.
4. Blackburn, E. H., C. W. Greider, and J. W. Szostak. 2006. Telomeres and telomerase: the path from maize, Tetrahymena and yeast to human cancer and aging. Nat. Med. 12:1133-1138.
5. Bodnar, A. G., N. W. Kim, R. B. Effros, and C.-P. Chiu. 1996. Mechanism of telomerase induction during T cell activation. Exp. Cell Res. 228:58-64.
6. Bryan, T. M., K. J. Goodrich, and T. R. Cech. 2003. Tetrahymena telomerase is active as a monomer. Mol. Biol. Cell 14:4794-4804.
7. Cech, T. R. 2004. Beginning to understand the end of the chromosome. Cell 116:273-279.
8. Cohen, S. B., M. E. Graham, G. O. Lovrecz, N. Bache, P. J. Robinson, and R. R. Reddel. 2007. Protein composition of catalytically active human telomerase from immortal cells. Science 315:1850-1853.
9. Collins, K. 2006. The biogenesis and regulation of telomerase holoenzymes. Nat. Rev. Mol. Cell Biol. 7:484-494.
10. Collins, K. 2008. Physiological assembly and activity of human telomerase complexes. Mech. Ageing Dev. 129:91-98.
11. Collins, K., and J. R. Mitchell. 2002. Telomerase in the human organism. Oncogene 21:564-579.
12. Cong, Y.-S., W. E. Wright, and J. W. Shay. 2002. Human telomerase and its regulation. Microbiol. Mol. Biol. Rev. 66:407-425.
13. Cristofari, G., and J. Lingner. 2006. Telomere length homeostasis requires that telomerase levels are limiting. EMBO J. 25:565-574.
14. Cunningham, D. D., and K. Collins. 2005. Biological and biochemical functions of RNA in the Tetrahymena telomerase holoenzyme. Mol. Cell. Biol. 25:4442-4454.
15. Feng, J., W. D. Funk, S. Wang, S. L. Weinrich, A. A. Avilion, C. Chiu, R. R. Adams, E. Chang, R. C. Allsopp, J. Yu, S. Le, M. West, C. B. Harley, W. H. Andrews, C. W. Greider, and B. Villeponteau. 1995. The RNA component of human telomerase. Science 269:1236-1241.
16. Fu, D., and K. Collins. 2003. Distinct biogenesis pathways for human telomerase RNA and H/ACA small nucleolar RNAs. Mol. Cell 11:1361-1372.
17. Fu, D., and K. Collins. 2007. Purification of human telomerase complexes identifies factors involved in telomerase biogenesis and telomere length regulation. Mol. Cell 28:773-785.
18. Garcia, C. K., W. E. Wright, and J. W. Shay. 2007. Human diseases of telomerase dysfunction: insights into tissue aging. Nucleic Acids Res. 35: 7406-7416.
19. Gilson, E., and V. Geli. 2007. How telomeres are replicated. Nat. Rev. Mol. Cell Biol. 8:825-838.
20. Greider, C. W. 2006. Telomerase RNA levels limit the telomere length equilibrium. Cold Spring Harbor Symp. Quant. Biol. 71:225-229.
21. Hogg, J. R., and K. Collins. 2007. RNA-based affinity purification reveals 7SK RNPs with distinct composition and regulation. RNA 13:868-880.
22. Hug, N., and J. Lingner. 2006. Telomere length homeostasis. Chromosoma 115:413-425.
23. Kapust, R. B., J. Tozser, J. D. Fox, D. E. Anderson, S. Cherry, T. D. Copeland, and D. S. Waugh. 2001. Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency. Protein Eng. 14:993-1000.
24. Lai, C. K., M. C. Miller, and K. Collins. 2003. Roles for RNA in telomerase nucleotide and repeat addition processivity. Mol. Cell 11:1673-1683.
25. Lai, C. K., J. R. Mitchell, and K. Collins. 2001. RNA binding domain of telomerase reverse transcriptase. Mol. Cell. Biol. 21:990-1000.
26. LeCuyer, K. A., L. S. Behlen, and O. C. Uhlenbeck. 1995. Mutants of the bacteriophage MS2 coat protein that alter its cooperative binding to RNA. Biochemistry 34:10600-10606.
27. Li, S., and E. H. Blackburn. 2006. Expression and suppression of human telomerase RNA. Cold Spring Harbor Symp. Quant. Biol. 71:211-215.
28. Lim, F., and D. S. Peabody. 2002. RNA recognition site of PP7 coat protein. Nucleic Acids Res. 30:4138-4144.
29. Livengood, A. J., A. J. Zaug, and T. R. Cech. 2002. Essential regions of Saccharomyces cerevisiae telomerase RNA: separate elements for Est1p and Est2p interaction. Mol. Cell. Biol. 22:2366-2374.
30. Marrone, A., D. Stevens, T. Vulliamy, I. Dokal, and P. J. Mason. 2004. Heterozygous telomerase RNA mutations found in dyskeratosis congenita and aplastic anemia reduce telomerase activity via haploinsufficiency. Blood 104:3936-3942.
31. Mitchell, J. R., J. Cheng, and K. Collins. 1999. A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 3' end. Mol. Cell. Biol. 19:567-576.
32. Mitchell, J. R., and K. Collins. 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. Mitchell, J. R., E. Wood, and K. Collins. 1999. A telomerase component is defective in the human disease dyskeratosis congenita. Nature 402:551-555.
34. Prowse, K. R., and C. W. Greider. 1995. Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proc. Natl. Acad. Sci. USA 92:4818-4822.
35. Tesmer, V. M., L. P. Ford, S. E. Holt, B. C. Frank, X. Yi, D. L. Aisner, M. Ouellette, J. W. Shay, and W. E. Wright. 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.
36. Theimer, C. A., C. A. BIois, and J. Feigon. 2005. Structure of the human telomerase RNA pseudoknot reveals conserved tertiary interactions essential for function. Mol. Cell 17:671-682.
37. Theimer, C. A., and J. Feigon. 2006. Structure and function of telomerase RNA. Curr. Opin. Struct. Biol. 16:307-318.
38. Ueda, C. T., and R. W. Roberts. 2004. Analysis of a long-range interaction between conserved domains of human telomerase RNA. RNA 10:139-147.
39. Verdun, R. E., and J. Karlseder. 2007. Replication and protection of telomeres. Nature 447:924-931.
40. Vulliamy, T. J., and I. Dokal. 2008. Dyskeratosis congenita: the diverse clinical presentation of mutations in the telomerase complex. Biochimie 90:122-130.
41. Vulliamy, T. J., A. Marrone, I. Dokal, and P. J. Mason. 2002. Association between aplastic anemia and mutations in telomerase RNA. Lancet 359: 2168-2170.
42. Vulliamy, T. J., A. Marrone, S. W. Knight, A. Walne, P. J. Mason, and I. Dokal. 2006. Mutations in dyskeratosis congenita: their impact on telomere length and the diversity of clinical presentation. Blood 107:2680-2685.
43. Weinrich, S. L., R. Pruzan, L. Ma, M. Ouellette, V. M. Tesmer, S. E. Holt, A. G. Bodnar, S. Lichsteiner, N. W. Kim, J. B. Trager, R. D. Taylor, R. Carlos, W. H. Andrews, W. E. Wright, J. W. Shay, C. B. Harley, and G. B. Morin. 1997. Reconstitution of human telomerase with the template RNA component hTR and the catalytic protein subunit hTRT. Nat. Genet. 17: 498-502.
44. Wenz, C., B. Enenkel, M. Amacker, C. Kelleher, K. Damm, and J. Lingner. 2001. Human telomerase contains two cooperating telomerase RNA molecules. EMBO J. 20:3526-3534.
45. Westin, E. R., E. Chavez, K. M. Lee, F. A. Gourronc, S. Riley, P. M. Lansdorp, F. D. Goldman, and A. J. Klingelhutz. 2007. Telomere restoration and extension of proliferative lifespan in dyskeratosis congenita fibroblasts. Aging Cell 6:383-394.
46. Wilson, D. B., J. Ivanovich, A. Whelan, P. J. Goodfellow, and M. Bessler. 2003. Human telomerase RNA mutations and bone marrow failure. Lancet 361:1993-1994.
47. Witkin, K. L., and K. Collins. 2004. Holoenzyme proteins required for the physiological assembly and activity of telomerase. Genes Dev. 18:1107-1118.
48. Wong, J. M., M. J. Kyasa, L. Hutchins, and K. Collins. 2004. Telomerase RNA deficiency in peripheral blood mononuclear cells in X-linked dyskeratosis congenita. Hum. Genet. 115:448-455.
49. Wong, J. M. Y., and K. Collins. 2006. Telomerase RNA level limits telomere maintenance in X-linked dyskeratosis congenita. Genes Dev. 20:2848-2858.
50. Wong, J. M. Y., and K. Collins. 2003. Telomere maintenance and disease. Lancet 362:983-988.
51. Xin, Z. T., A. D. Beauchamp, R. T. Calado, J. W. Bradford, J. A. Regal, A. Shenoy, Y. Liang, P. M. Lansdorp, N. S. Young, and H. Ly. 2007. Functional characterization of natural telomerase mutations found in patients with hematologic disorders. Blood 109:524-532.
52. Yamaguchi, H., G. M. Baerlocher, P. M. Lansdorp, S. J. Chanock, O. Nunez, E. Sloand, and N. S. Young. 2003. Mutations of the human telomerase RNA gene (TERC) in aplastic anemia and myelodysplastic syndrome. Blood 102: 916-918.
53. Yi, X., V. M. Tesmer, I. Savre-Train, J. W. Shay, and W. E. Wright. 1999. Both transcriptional and post transcriptional mechanisms regulate human telomerase template RNA levels. Mol. Cell. Biol. 19:3989-3997.
54. Yu, G., and E. H. Blackburn. 1991. Developmentally programmed healing of chromosomes by telomerase in Tetrahymena. Cell 67:823-832.