Contributions of the TEL-patch amino acid cluster on TPP1 to Telomeric DNA synthesis by human telomerase

Journal of Molecular Biology

Volumn 427, Issue 6, 2015, Pages 1291-1303

  Dalby, Andrew B ^a   Hofr, Ctirad ^b   Cech, Thomas R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b MASARYK UNIVERSITY   (Czech Republic)

Author keywords

DNA substrate competition; processivity; telomerase recruitment; telomere; TPP1 TEL patch

Indexed keywords

AMINO ACID; DEOXYADENOSINE TRIPHOSPHATE; DEOXYGUANOSINE TRIPHOSPHATE; PEPTIDES AND PROTEINS; POT1 PROTEIN; SINGLE STRANDED DNA; TEL PATCH AMINO ACID CLUSTER; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TPP1 PROTEIN; UNCLASSIFIED DRUG; AMINOPEPTIDASE; DIPEPTIDYL PEPTIDASE; DNA; PROTEIN BINDING; SERINE PROTEINASE; TERT PROTEIN, HUMAN; TRIPEPTIDYL-PEPTIDASE 1;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION; DISSOCIATION CONSTANT; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; GENE MUTATION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING; BINDING COMPETITION; CHEMICAL STRUCTURE; DNA REPLICATION; GEL MOBILITY SHIFT ASSAY; GENETICS; HEK293 CELL LINE; METABOLISM; PROTEIN TRANSPORT; TELOMERE;

AMINO ACIDS; AMINOPEPTIDASES; BINDING, COMPETITIVE; DIPEPTIDYL-PEPTIDASES AND TRIPEPTIDYL-PEPTIDASES; DNA; DNA REPLICATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN TRANSPORT; SERINE PROTEASES; TELOMERASE; TELOMERE;

EID: 84924107491     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.01.008     Document Type: Article

References (62)

1. T.R. Cech Beginning to understand the end of the chromosome Cell 116 2004 273 279
2. J. Nandakumar, and T.R. Cech Finding the end: recruitment of telomerase to telomeres Nat Rev Mol Cell Biol 14 2013 69 82
3. L.F. Batista, and S.E. Artandi Understanding telomere diseases through analysis of patient-derived iPS cells Curr Opin Genet Dev 23 2013 526 533
4. M.Z. Levy, R.C. Allsopp, A.B. Futcher, C.W. Greider, and C.B. Harley Telomere end-replication problem and cell aging J Mol Biol 225 1992 951 960
5. S.A. Stewart, and R.A. Weinberg Telomeres: cancer to human aging Annu Rev Cell Dev Biol 22 2006 531 557
6. J.W. Shay, and W.E. Wright Role of telomeres and telomerase in cancer Semin Cancer Biol 21 2011 349 353
7. M. Armanios, and E.H. Blackburn The telomere syndromes Nat Rev Genet 13 2012 693 704
8. B. Holohan, W.E. Wright, and J.W. Shay Cell biology of disease: telomeropathies: an emerging spectrum disorder J Cell Biol 205 2014 289 299
9. C.W. Greider, and E.H. Blackburn A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis Nature 337 1989 331 337
10. J. Lingner, T.R. Hughes, A. Shevchenko, M. Mann, V. Lundblad, and T.R. Cech Reverse transcriptase motifs in the catalytic subunit of telomerase Science 276 1997 561 567
11. T.M. Nakamura, G.B. Morin, K.B. Chapman, S.L. Weinrich, W.H. Andrews, and J. Lingner Telomerase catalytic subunit homologs from fission yeast and human Science 277 1997 955 959
12. J.L. Chen, M.A. Blasco, and C.W. Greider Secondary structure of vertebrate telomerase RNA Cell 100 2000 503 514
13. V.M. Tesmer, L.P. Ford, S.E. Holt, B.C. Frank, X. Yi, and D.L. Aisner 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 1999 6207 6216
14. J. Jurczyluk, A.S. Nouwens, J.K. Holien, T.E. Adams, G.O. Lovrecz, and M.W. Parker Direct involvement of the TEN domain at the active site of human telomerase Nucleic Acids Res 39 2011 1774 1788
15. R.A. Wu, and K. Collins Human telomerase specialization for repeat synthesis by unique handling of primer-template duplex EMBO J 33 2014 921 935
16. A.R. Robart, and K. Collins Human telomerase domain interactions capture DNA for TEN domain-dependent processive elongation Mol Cell 42 2011 308 318
17. S. Huard, T.J. Moriarty, and C. Autexier The C terminus of the human telomerase reverse transcriptase is a determinant of enzyme processivity Nucleic Acids Res 31 2003 4059 4070
18. M. Xie, J.D. Podlevsky, X. Qi, C.J. Bley, and J.J. Chen A novel motif in telomerase reverse transcriptase regulates telomere repeat addition rate and processivity Nucleic Acids Res 38 2010 1982 1996
19. S.N. Finger, and T.M. Bryan Multiple DNA-binding sites in Tetrahymena telomerase Nucleic Acids Res 36 2008 1260 1272
20. J.R. Mitchell, E. Wood, and K. Collins A telomerase component is defective in the human disease dyskeratosis congenita Nature 402 1999 551 555
21. A.S. Venteicher, E.B. Abreu, Z. Meng, K.E. McCann, R.M. Terns, and T.D. Veenstra A human telomerase holoenzyme protein required for Cajal body localization and telomere synthesis Science 323 2009 644 648
22. B.E. Jady, E. Bertrand, and T. Kiss Human telomerase RNA and box H/ACA scaRNAs share a common Cajal body-specific localization signal J Cell Biol 164 2004 647 652
23. B.E. Jady, P. Richard, E. Bertrand, and T. Kiss Cell cycle-dependent recruitment of telomerase RNA and Cajal bodies to human telomeres Mol Biol Cell 17 2006 944 954
24. R.L. Tomlinson, T.D. Ziegler, T. Supakorndej, R.M. Terns, and M.P. Terns Cell cycle-regulated trafficking of human telomerase to telomeres Mol Biol Cell 17 2006 955 965
25. E. Abreu, E. Aritonovska, P. Reichenbach, G. Cristofari, B. Culp, and R.M. Terns TIN2-tethered TPP1 recruits human telomerase to telomeres in vivo Mol Cell Biol 30 2010 2971 2982
26. H. Xin, D. Liu, M. Wan, A. Safari, H. Kim, and W. Sun TPP1 is a homologue of ciliate TEBP-beta and interacts with POT1 to recruit telomerase Nature 445 2007 559 562
27. L. Xi, and T.R. Cech Inventory of telomerase components in human cells reveals multiple subpopulations of hTR and hTERT Nucleic Acids Res 42 2014 8565 8577
28. C.B. Harley, A.B. Futcher, and C.W. Greider Telomeres shorten during aging of human fibroblasts Nature 345 1990 458 460
29. Y. Zhao, E. Abreu, J. Kim, G. Stadler, U. Eskiocak, and M.P. Terns Processive and distributive extension of human telomeres by telomerase under homeostatic and nonequilibrium conditions Mol Cell 42 2011 297 307
30. A.J. Zaug, S.M. Crary, M. Jesse Fioravanti, K. Campbell, and T.R. Cech Many disease-associated variants of hTERT retain high telomerase enzymatic activity Nucleic Acids Res 41 2013 8969 8978
31. T. de Lange Shelterin: the protein complex that shapes and safeguards human telomeres Genes Dev 19 2005 2100 2110
32. E.L. Denchi, and T. de Lange Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1 Nature 448 2007 1068 1071
33. A. Sfeir, and T. de Lange Removal of shelterin reveals the telomere end-protection problem Science 336 2012 593 597
34. D. Loayza, and T. De Lange POT1 as a terminal transducer of TRF1 telomere length control Nature 423 2003 1013 1018
35. M. Lei, A.J. Zaug, E.R. Podell, and T.R. Cech Switching human telomerase on and off with hPOT1 protein in vitro J Biol Chem 280 2005 20449 20456
36. J. Nandakumar, C.F. Bell, I. Weidenfeld, A.J. Zaug, L.A. Leinwand, and T.R. Cech The TEL patch of telomere protein TPP1 mediates telomerase recruitment and processivity Nature 492 2012 285 289
37. F.L. Zhong, L.F. Batista, A. Freund, M.F. Pech, A.S. Venteicher, and S.E. Artandi TPP1 OB-fold domain controls telomere maintenance by recruiting telomerase to chromosome ends Cell 150 2012 481 494
38. A.N. Sexton, S.G. Regalado, C.S. Lai, G.J. Cost, C.M. O'Neil, and F.D. Urnov Genetic and molecular identification of three human TPP1 functions in telomerase action: recruitment, activation, and homeostasis set point regulation Genes Dev 28 2014 1885 1899
39. M. Nakashima, J. Nandakumar, K.D. Sullivan, J.M. Espinosa, and T.R. Cech Inhibition of telomerase recruitment and cancer cell death J Biol Chem 288 2013 33171 33180
40. J.C. Schmidt, A.B. Dalby, and T.R. Cech Identification of human TERT elements necessary for telomerase recruitment to telomeres eLife 2014 3 10.7554/eLife.03563
41. F. Wang, E.R. Podell, A.J. Zaug, Y. Yang, P. Baciu, and T.R. Cech The POT1-TPP1 telomere complex is a telomerase processivity factor Nature 445 2007 506 510
42. C.M. Latrick, and T.R. Cech POT1-TPP1 enhances telomerase processivity by slowing primer dissociation and aiding translocation EMBO J 29 2010 924 933
43. Y. D'Souza, T.W. Chu, and C. Autexier A translocation-defective telomerase with low levels of activity and processivity stabilizes short telomeres and confers immortalization Mol Biol Cell 24 2013 1469 1479
44. X. Qi, M. Xie, A.F. Brown, C.J. Bley, J.D. Podlevsky, and J.J. Chen RNA/DNA hybrid binding affinity determines telomerase template-translocation efficiency EMBO J 31 2012 150 161
45. A. Fersht Enzyme structure and mechanism 1977 W. H. Freeman [Reading Eng] San Francisco
46. A.N. Sexton, D.T. Youmans, and K. Collins Specificity requirements for human telomere protein interaction with telomerase holoenzyme J Biol Chem 287 2012 34455 34464
47. C.K. Mathews DNA precursor metabolism and genomic stability FASEB J 20 2006 1300 1314
48. T.W. Traut Physiological concentrations of purines and pyrimidines Mol Cell Biochem 140 1994 1 22
49. C.W. Greider Telomerase is processive Mol Cell Biol 11 1991 4572 4580
50. A.J. Berman, B.M. Akiyama, M.D. Stone, and T.R. Cech The RNA accordion model for template positioning by telomerase RNA during telomeric DNA synthesis Nat Struct Mol Biol 18 2011 1371 1375
51. M.C. Miller, and K. Collins Telomerase recognizes its template by using an adjacent RNA motif Proc Natl Acad Sci USA 99 2002 6585 6590
52. A.J. Zaug, E.R. Podell, J. Nandakumar, and T.R. Cech Functional interaction between telomere protein TPP1 and telomerase Genes Dev 24 2010 613 622
53. T.M. Bryan, K.J. Goodrich, and T.R. Cech A mutant of Tetrahymena telomerase reverse transcriptase with increased processivity J Biol Chem 275 2000 24199 24207
54. K.K. Takai, S. Hooper, S. Blackwood, R. Gandhi, and T. de Lange In vivo stoichiometry of shelterin components J Biol Chem 285 2010 1457 1467
55. M. Rajavel, M.R. Mullins, and D.J. Taylor Multiple facets of TPP1 in telomere maintenance Biochim Biophys Acta 2014 1844 1550 1559
56. H. Hwang, N. Buncher, P.L. Opresko, and S. Myong POT1-TPP1 regulates telomeric overhang structural dynamics Structure 20 2012 1872 1880
57. K.D. Tsakiri, J.T. Cronkhite, P.J. Kuan, C. Xing, G. Raghu, and J.C. Weissler Adult-onset pulmonary fibrosis caused by mutations in telomerase Proc Natl Acad Sci USA 104 2007 7552 7557
58. Y. Guo, M. Kartawinata, J. Li, H.A. Pickett, J. Teo, and T. Kilo Inherited bone marrow failure associated with germline mutation of ACD, the gene encoding telomere protein TPP1 Blood 124 2014 2767 2774
59. H. Kocak, B.J. Ballew, K. Bisht, R. Eggebeen, B.D. Hicks, and S. Suman Hoyeraal-Hreidarsson syndrome caused by a germline mutation in the TEL patch of the telomere protein TPP1 Genes Dev 2014 10.1101/gad.248567.114
60. A. Sauerwald, S. Sandin, G. Cristofari, S.H. Scheres, J. Lingner, and D. Rhodes Structure of active dimeric human telomerase Nat Struct Mol Biol 20 2013 454 460
61. G. Cristofari, and J. Lingner Telomere length homeostasis requires that telomerase levels are limiting EMBO J 25 2006 565 574
62. M. Lei, E.R. Podell, and T.R. Cech Structure of human POT1 bound to telomeric single-stranded DNA provides a model for chromosome end-protection Nat Struct Mol Biol 11 2004 1223 1229