Structure of the Human Telomeric Stn1-Ten1 Capping Complex

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Bryan, Christopher ^a,b   Rice, Cory ^a,b   Harkisheimer, Michael ^a   Schultz, David C ^a   Skordalakes, Emmanuel ^a,b  

^a WISTAR INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN A; STN1 TEN1 PROTEIN; UNCLASSIFIED DRUG; PROTEIN BINDING; STN1 PROTEIN, HUMAN; TELOMERE BINDING PROTEIN; TEN1 PROTEIN, HUMAN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CAPPING PHENOMENON; CARBOXY TERMINAL SEQUENCE; CELL ASSAY; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; HUMAN; HUMAN CELL; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; TELOMERE; CHEMISTRY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE;

EUKARYOTA;

HUMANS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; TELOMERE; TELOMERE-BINDING PROTEINS;

EID: 84879468648     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066756     Document Type: Article

References (57)

1. Blackburn EH, Gall JG, (1978) A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol 120: 33-53.
2. de Lange T, (2009) How telomeres solve the end-protection problem. Science 326: 948-952.
3. Baumann P, Podell E, Cech TR, (2002) Human Pot1 (protection of telomeres) protein: cytolocalization, gene structure, and alternative splicing. Molecular and cellular biology 22: 8079-8087.
4. Miyake Y, Nakamura M, Nabetani A, Shimamura S, Tamura M, et al. (2009) RPA-like mammalian Ctc1-Stn1-Ten1 complex binds to single-stranded DNA and protects telomeres independently of the Pot1 pathway. Molecular cell 36: 193-206.
5. Wellinger RJ, (2009) The CST complex and telomere maintenance: the exception becomes the rule. Molecular cell 36: 168-169.
6. de Lange T, (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19: 2100-2110.
7. Pennock E, Buckley K, Lundblad V, (2001) Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104: 387-396.
8. Evans SK, Lundblad V, (1999) Est1 and Cdc13 as Comediators of Telomerase Access. Science 286: 117-120.
9. Grandin N, Damon C, Charbonneau M, (2001) Cdc13 prevents telomere uncapping and Rad50-dependent homologous recombination. The EMBO journal 20: 6127-6139.
10. Puglisi A, Bianchi A, Lemmens L, Damay P, Shore D, (2008) Distinct roles for yeast Stn1 in telomere capping and telomerase inhibition. The EMBO journal 27: 2328-2339.
11. Gao H, Cervantes RB, Mandell EK, Otero JH, Lundblad V, (2007) RPA-like proteins mediate yeast telomere function. Nature structural & molecular biology 14: 208-214.
12. Qian W, Fu XH, Zhou JQ, (2010) Purification and characterization of Stn1p, a single-stranded telomeric DNA binding protein. Protein expression and purification 73: 107-112.
13. Qian W, Wang J, Jin NN, Fu XH, Lin YC, et al. (2009) Ten1p promotes the telomeric DNA-binding activity of Cdc13p: implication for its function in telomere length regulation. Cell Res 19: 849-863.
14. Chandra A, Hughes TR, Nugent CI, Lundblad V, (2001) Cdc13 both positively and negatively regulates telomere replication. Genes Dev 15: 404-414.
15. DeZwaan DC, Toogun OA, Echtenkamp FJ, Freeman BC, (2009) The Hsp82 molecular chaperone promotes a switch between unextendable and extendable telomere states. Nature structural & molecular biology 16: 711-716.
16. Li S, Makovets S, Matsuguchi T, Blethrow JD, Shokat KM, et al. (2009) Cdk1-dependent phosphorylation of Cdc13 coordinates telomere elongation during cell-cycle progression. Cell 136: 50-61.
17. Tseng SF, Lin JJ, Teng SC, (2006) The telomerase-recruitment domain of the telomere binding protein Cdc13 is regulated by Mec1p/Tel1p-dependent phosphorylation. Nucleic acids research 34: 6327-6336.
18. Petreaca RC, Chiu H-C, Eckelhoefer HA, Chuang C, Xu L, et al. (2006) Chromosome end protection plasticity revealed by Stn1p and Ten1p bypass of Cdc13p. Nat Cell Biol 8: 748-755.
19. Garvik B, Carson M, Hartwell L, (1995) Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Molecular cell 15: 6128-6138.
20. Bianchi A, Negrini S, Shore D, (2004) Delivery of Yeast Telomerase to a DNA Break Depends on the Recruitment Functions of Cdc13 and Est1. Molecular cell 16: 139-146.
21. Lydall D, Weinert T, (1995) Yeast checkpoint genes in DNA damage processing: implications for repair and arrest. Science 270: 1488-1491.
22. Lin JJ, Zakian VA, (1996) The Saccharomyces CDC13 protein is a single-strand TG1-3 telomeric DNA-binding protein in vitro that affects telomere behavior in vivo. Proceedings of the National Academy of Sciences of the United States of America 93: 13760-13765.
23. Nugent CI, Hughes TR, Lue NF, Lundblad V, (1996) Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274: 249-252.
24. Grandin N, Damon C, Charbonneau M, (2001) Ten1 functions in telomere end protection and length regulation in association with Stn1 and Cdc13. The EMBO journal 20: 1173-1183.
25. Martin V, Du LL, Rozenzhak S, Russell P, (2007) Protection of telomeres by a conserved Stn1-Ten1 complex. Proceedings of the National Academy of Sciences of the United States of America 104: 14038-14043.
26. Surovtseva YV, Churikov D, Boltz KA, Song X, Lamb JC, et al. (2009) Conserved telomere maintenance component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Molecular cell 36: 207-218.
27. Gu P, Min JN, Wang Y, Huang C, Peng T, et al. (2012) CTC1 deletion results in defective telomere replication, leading to catastrophic telomere loss and stem cell exhaustion. The EMBO journal 31: 2309-2321.
28. Chen LY, Redon S, Lingner J, (2012) The human CST complex is a terminator of telomerase activity. Nature 488(7412): 540544.
29. Nakaoka H, Nishiyama A, Saito M, Ishikawa F, (2012) Xenopus laevis Ctc1-Stn1-Ten1 (xCST) protein complex is involved in priming DNA synthesis on single-stranded DNA template in Xenopus egg extract. The Journal of biological chemistry 287: 619-627.
30. Casteel DE, Zhuang S, Zeng Y, Perrino FW, Boss GR, et al. (2009) A DNA polymerase-{alpha}{middle dot}primase cofactor with homology to replication protein A-32 regulates DNA replication in mammalian cells. The Journal of biological chemistry 284: 5807-5818.
31. Huang C, Dai X, Chai W, (2012) Human Stn1 protects telomere integrity by promoting efficient lagging-strand synthesis at telomeres and mediating C-strand fill-in. Cell Res 22(12): 1681-1695.
32. Song X, Leehy K, Warrington RT, Lamb JC, Surovtseva YV, et al. (2008) STN1 protects chromosome ends in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 105: 19815-19820.
33. Stewart JA, Wang F, Chaiken MF, Kasbek C, Chastain PD 2nd, et al (2012) Human CST promotes telomere duplex replication and general replication restart after fork stalling. The EMBO journal 31: 3537-3549.
34. Sun J, Yu EY, Yang Y, Confer LA, Sun SH, et al. (2009) Stn1-Ten1 is an Rpa2-Rpa3-like complex at telomeres. Genes Dev 23: 2900-2914.
35. Gelinas AD, Paschini M, Reyes FE, Heroux A, Batey RT, et al. (2009) Telomere capping proteins are structurally related to RPA with an additional telomere-specific domain. Proceedings of the National Academy of Sciences of the United States of America 106: 19298-19303.
36. Holm L, Rosenström P, (2010) Dali server: conservation mapping in 3D. Nucl Acids Res 38: W545-549.
37. Bochkareva E, Korolev S, Lees-Miller SP, Bochkarev A, (2002) Structure of the RPA trimerization core and its role in the multistep DNA-binding mechanism of RPA. The EMBO journal 21: 1855-1863.
38. Brush GS, Morrow DM, Hieter P, Kelly TJ, (1996) The ATM homologue MEC1 is required for phosphorylation of replication protein A in yeast. Proceedings of the National Academy of Sciences of the United States of America 93: 15075-15080.
39. Dornreiter I, Erdile LF, Gilbert IU, von Winkler D, Kelly TJ, et al. (1992) Interaction of DNA polymerase alpha-primase with cellular replication protein A and SV40 T antigen. The EMBO journal 11: 769-776.
40. Kenny MK, Lee SH, Hurwitz J, (1989) Multiple functions of human single-stranded-DNA binding protein in simian virus 40 DNA replication: single-strand stabilization and stimulation of DNA polymerases alpha and delta. Proceedings of the National Academy of Sciences of the United States of America 86: 9757-9761.
41. Ivessa AS, Zhou JQ, Schulz VP, Monson EK, Zakian VA, (2002) Saccharomyces Rrm3p, a 5' to 3' DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev 16: 1383-1396.
42. Makovets S, Herskowitz I, Blackburn EH, (2004) Anatomy and dynamics of DNA replication fork movement in yeast telomeric regions. Molecular and cellular biology 24: 4019-4031.
43. Miller KM, Rog O, Cooper JP, (2006) Semi-conservative DNA replication through telomeres requires Taz1. Nature 440: 824-828.
44. Dart DA, Adams KE, Akerman I, Lakin ND, (2004) Recruitment of the cell cycle checkpoint kinase ATR to chromatin during S-phase. The Journal of biological chemistry 279: 16433-16440.
45. Taggart AK, Teng SC, Zakian VA, (2002) Est1p as a cell cycle-regulated activator of telomere-bound telomerase. Science 297: 1023-1026.
46. Wellinger RJ, Wolf AJ, Zakian VA, (1993) Saccharomyces telomeres acquire single-strand TG1-3 tails late in S phase. Cell 72: 51-60.
47. Xu L, Petreaca RC, Gasparyan HJ, Vu S, Nugent CI, (2009) TEN1 is essential for CDC13-mediated telomere capping. Genetics 183: 793-810.
48. Fanning E, Klimovich V, Nager AR, (2006) A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic acids research 34: 4126-4137.
49. Fan J, Pavletich NP, (2012) Structure and conformational change of a replication protein A heterotrimer bound to ssDNA. Genes & development 26: 2337-2347.
50. Kelley LA, Sternberg MJ, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
51. Terwilliger TC, Berendzen J, (1999) Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 55: 849-861.
52. Otwinowski Z (1991) Isomorphous Scattering and Anomalous Replacement. Warrington: Daresbury Laboratory.
53. Terwilliger T, (2003) Automated main-chain model building by template matching and iterative fragment extension. Acta Crystallographica Section D 59: 38-44.
54. Terwilliger TC, (2000) Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr 56: 965-972.
55. Emsley P, Cowtan KD (2004) Acta Cryst D60. Acta Crystallogr D Biol Crystallogr: 2126-2132.
56. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of Macromolecular Structures by the Maximum-Likelihood Method. Acta Crystallographica Section D 53: 240-255.
57. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.