Interplay between nonsense-mediated mRNA decay and DNA damage response pathways reveals that Stn1 and Ten1 are the key CST telomere-cap components

Cell Reports

Volumn 7, Issue 4, 2014, Pages 1259-1269

  Holstein, Eva Maria ^a   Clark, Kate R M ^a   Lydall, David ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DNA; DOUBLE STRANDED DNA; MESSENGER RNA; NUCLEOPROTEIN; PROTEIN; SINGLE STRANDED DNA; STN1 PROTEIN; TEN1 PROTEIN; UNCLASSIFIED DRUG; NUCLEAR PROTEIN; PROTEIN CDC 13; PROTEIN STN1; PROTEIN TEN1; CELL CYCLE PROTEIN; NONHISTONE PROTEIN; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN; STN1 PROTEIN, S CEREVISIAE; TELOMERE BINDING PROTEIN; TEN1 PROTEIN, S CEREVISIAE;

ARTICLE; CANDIDA GLABRATA; DNA DAMAGE; DNA REPLICATION; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; STOICHIOMETRY; TELOMERE; YEAST; CDC13 GENE; CELL VIABILITY; CONTROLLED STUDY; GENE DELETION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE LOCATION; GENE OVEREXPRESSION; KNOCKOUT GENE; PROTEIN LOCALIZATION; STN1 GENE; TELOMERE CAPPING; TEN1 GENE; GENETICS; METABOLISM; PROTEIN SECONDARY STRUCTURE;

EUKARYOTA; MAMMALIA;

CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA DAMAGE; DNA, SINGLE-STRANDED; NONSENSE MEDIATED MRNA DECAY; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERE; TELOMERE-BINDING PROTEINS; YEASTS;

EID: 84901274143     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.04.017     Document Type: Article

References (54)

1. Addinall S.G., Holstein E.M., Lawless C., Yu M., Chapman K., Banks A.P., Ngo H.P., Maringele L., Taschuk M., Young A., et al. Quantitative fitness analysis shows that NMD proteins and many other protein complexes suppress or enhance distinct telomere cap defects. PLoS Genet. 2011, 7:e1001362.
2. Anderson B.H., Kasher P.R., Mayer J., Szynkiewicz M., Jenkinson E.M., Bhaskar S.S., Urquhart J.E., Daly S.B., Dickerson J.E., O'Sullivan J., et al. Mutations in CTC1, encoding conserved telomere maintenance component 1, cause Coats plus. Nat. Genet. 2012, 44:338-342.
3. Azzalin C.M., Reichenbach P., Khoriauli L., Giulotto E., Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007, 318:798-801.
4. Ben-Shitrit T., Yosef N., Shemesh K., Sharan R., Ruppin E., Kupiec M. Systematic identification of gene annotation errors in the widely used yeast mutation collections. Nat. Methods 2012, 9:373-378.
5. Bidou L., Allamand V., Rousset J.P., Namy O. Sense from nonsense: therapies for premature stop codon diseases. Trends Mol. Med. 2012, 18:679-688.
6. Bunting S.F., Callén E., Wong N., Chen H.T., Polato F., Gunn A., Bothmer A., Feldhahn N., Fernandez-Capetillo O., Cao L., et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 2010, 141:243-254.
7. Casteel D.E., Zhuang S., Zeng Y., Perrino F.W., Boss G.R., Goulian M., Pilz R.B. A DNA polymerase-αmiddle dotprimase cofactor with homology to replication protein A-32 regulates DNA replication in mammalian cells. J. Biol. Chem. 2009, 284:5807-5818.
8. Chandra A., Hughes T.R., Nugent C.I., Lundblad V. Cdc13 both positively and negatively regulates telomere replication. Genes Dev. 2001, 15:404-414.
9. Chen L.Y., Redon S., Lingner J. The human CST complex is a terminator of telomerase activity. Nature 2012, 488:540-544.
10. Chen L.Y., Majerská J., Lingner J. Molecular basis of telomere syndrome caused by CTC1 mutations. Genes Dev. 2013, 27:2099-2108.
11. Collart M.A., Oliviero S. Preparation of yeast RNA. Curr. Protoc. Mol. Biol. 2001, Published online May 1, 2001. 10.1002/0471142727.mb1312s23.
12. Dahlseid J.N., Lew-Smith J., Lelivelt M.J., Enomoto S., Ford A., Desruisseaux M., McClellan M., Lue N., Culbertson M.R., Berman J. mRNAs encoding telomerase components and regulators are controlled by UPF genes in Saccharomyces cerevisiae. Eukaryot. Cell 2003, 2:134-142.
13. Dewar J.M., Lydall D. Pif1- and Exo1-dependent nucleases coordinate checkpoint activation following telomere uncapping. EMBO J. 2010, 29:4020-4034.
14. Dewar J.M., Lydall D. Simple, non-radioactive measurement of single-stranded DNA at telomeric, sub-telomeric, and genomic loci in budding yeast. Methods Mol. Biol. 2012, 920:341-348.
15. Dubarry M., Loïodice I., Chen C.L., Thermes C., Taddei A. Tight protein-DNA interactions favor gene silencing. Genes Dev. 2011, 25:1365-1370.
16. Gao H., Cervantes R.B., Mandell E.K., Otero J.H., Lundblad V. RPA-like proteins mediate yeast telomere function. Nat. Struct. Mol. Biol. 2007, 14:208-214.
17. Garvik B., Carson M., Hartwell L. Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol. Cell. Biol. 1995, 15:6128-6138.
18. Gasparyan H.J., Xu L., Petreaca R.C., Rex A.E., Small V.Y., Bhogal N.S., Julius J.A., Warsi T.H., Bachant J., Aparicio O.M., Nugent C.I. Yeast telomere capping protein Stn1 overrides DNA replication control through the S phase checkpoint. Proc. Natl. Acad. Sci. USA 2009, 106:2206-2211.
19. Giraud-Panis M.J., Teixeira M.T., Géli V., Gilson E. CST meets shelterin to keep telomeres in check. Mol. Cell 2010, 39:665-676.
20. Goldstein A.L., McCusker J.H. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 1999, 15:1541-1553.
21. Grandin N., Damon C., Charbonneau M. Ten1 functions in telomere end protection and length regulation in association with Stn1 and Cdc13. EMBO J. 2001, 20:1173-1183.
22. Greenall A., Lei G., Swan D.C., James K., Wang L., Peters H., Wipat A., Wilkinson D.J., Lydall D. A genome wide analysis of the response to uncapped telomeres in budding yeast reveals a novel role for the NAD+ biosynthetic gene BNA2 in chromosome end protection. Genome Biol. 2008, 9:R146.
23. Grossi S., Puglisi A., Dmitriev P.V., Lopes M., Shore D. Pol12, the B subunit of DNA polymerase alpha, functions in both telomere capping and length regulation. Genes Dev. 2004, 18:992-1006.
24. Gu P., Chang S. Functional characterization of human CTC1 mutations reveals novel mechanisms responsible for the pathogenesis of the telomere disease Coats plus. Aging Cell 2013, 12:1100-1109.
25. Guan Q., Zheng W., Tang S., Liu X., Zinkel R.A., Tsui K.W., Yandell B.S., Culbertson M.R. Impact of nonsense-mediated mRNA decay on the global expression profile of budding yeast. PLoS Genet. 2006, 2:e203.
26. Holstein E.M., Lydall D. Quantitative amplification of single-stranded DNA. Methods Mol. Biol. 2012, 920:323-339.
27. Isken O., Maquat L.E. The multiple lives of NMD factors: balancing roles in gene and genome regulation. Nat. Rev. Genet. 2008, 9:699-712.
28. Jain D., Cooper J.P. Telomeric strategies: means to an end. Annu. Rev. Genet. 2010, 44:243-269.
29. Lazzaro F., Sapountzi V., Granata M., Pellicioli A., Vaze M., Haber J.E., Plevani P., Lydall D., Muzi-Falconi M. Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J. 2008, 27:1502-1512.
30. Lew J.E., Enomoto S., Berman J. Telomere length regulation and telomeric chromatin require the nonsense-mediated mRNA decay pathway. Mol. Cell. Biol. 1998, 18:6121-6130.
31. Lewis K.A., Pfaff D.A., Earley J.N., Altschuler S.E., Wuttke D.S. The tenacious recognition of yeast telomere sequence by Cdc13 is fully exerted by a single OB-fold domain. Nucleic Acids Res. 2014, 42:475-484.
32. Lue N.F., Zhou R., Chico L., Mao N., Steinberg-Neifach O., Ha T. The telomere capping complex CST has an unusual stoichiometry, makes multipartite interaction with G-Tails, and unfolds higher-order G-tail structures. PLoS Genet. 2013, 9:e1003145.
33. Lundblad V., Blackburn E.H. An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell 1993, 73:347-360.
34. Maringele L., Lydall D. EXO1 plays a role in generating type I and type II survivors in budding yeast. Genetics 2004, 166:1641-1649.
35. Mitton-Fry R.M., Anderson E.M., Theobald D.L., Glustrom L.W., Wuttke D.S. Structural basis for telomeric single-stranded DNA recognition by yeast Cdc13. J. Mol. Biol. 2004, 338:241-255.
36. Miyake Y., Nakamura M., Nabetani A., Shimamura S., Tamura M., Yonehara S., Saito M., Ishikawa F. RPA-like mammalian Ctc1-Stn1-Ten1 complex binds to single-stranded DNA and protects telomeres independently of the Pot1 pathway. Mol. Cell 2009, 36:193-206.
37. Nakaoka H., Nishiyama A., Saito M., Ishikawa F. Xenopus laevis Ctc1-Stn1-Ten1 (xCST) protein complex is involved in priming DNA synthesis on single-stranded DNA template in Xenopus egg extract. J. Biol. Chem. 2012, 287:619-627.
38. Nugent C.I., Hughes T.R., Lue N.F., Lundblad V. Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 1996, 274:249-252.
39. Paschini M., Toro T.B., Lubin J.W., Braunstein-Ballew B., Morris D.K., Lundblad V. A naturally thermolabile activity compromises genetic analysis of telomere function in Saccharomyces cerevisiae. Genetics 2012, 191:79-93.
40. Petreaca R.C., Chiu H.C., Eckelhoefer H.A., Chuang C., Xu L., Nugent C.I. Chromosome end protection plasticity revealed by Stn1p and Ten1p bypass of Cdc13p. Nat. Cell Biol. 2006, 8:748-755.
41. Petreaca R.C., Chiu H.C., Nugent C.I. The role of Stn1p in Saccharomyces cerevisiae telomere capping can be separated from its interaction with Cdc13p. Genetics 2007, 177:1459-1474.
42. Polvi A., Linnankivi T., Kivelä T., Herva R., Keating J.P., Mäkitie O., Pareyson D., Vainionpää L., Lahtinen J., Hovatta I., et al. Mutations in CTC1, encoding the CTS telomere maintenance complex component 1, cause cerebroretinal microangiopathy with calcifications and cysts. Am. J. Hum. Genet. 2012, 90:540-549.
43. Puglisi A., Bianchi A., Lemmens L., Damay P., Shore D. Distinct roles for yeast Stn1 in telomere capping and telomerase inhibition. EMBO J. 2008, 27:2328-2339.
44. Qi H., Zakian V.A. The Saccharomyces telomere-binding protein Cdc13p interacts with both the catalytic subunit of DNA polymerase alpha and the telomerase-associated est1 protein. Genes Dev. 2000, 14:1777-1788.
45. Qian W., Wang J., Jin N.N., Fu X.H., Lin Y.C., Lin J.J., Zhou J.Q. Ten1p promotes the telomeric DNA-binding activity of Cdc13p: implication for its function in telomere length regulation. Cell Res. 2009, 19:849-863.
46. Qian W., Fu X.H., Zhou J.Q. Purification and characterization of Stn1p, a single-stranded telomeric DNA binding protein. Protein Expr. Purif. 2010, 73:107-112.
47. Sun J., Yu E.Y., Yang Y., Confer L.A., Sun S.H., Wan K., Lue N.F., Lei M. Stn1-Ten1 is an Rpa2-Rpa3-like complex at telomeres. Genes Dev. 2009, 23:2900-2914.
48. Sun J., Yang Y., Wan K., Mao N., Yu T.Y., Lin Y.C., DeZwaan D.C., Freeman B.C., Lin J.J., Lue N.F., Lei M. Structural bases of dimerization of yeast telomere protein Cdc13 and its interaction with the catalytic subunit of DNA polymerase α. Cell Res. 2011, 21:258-274.
49. Surovtseva Y.V., Churikov D., Boltz K.A., Song X., Lamb J.C., Warrington R., Leehy K., Heacock M., Price C.M., Shippen D.E. Conserved telomere maintenance component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Mol. Cell 2009, 36:207-218.
50. Walne A., Bhagat T., Kirwan M., Gitaux C., Desguerre I., Leonard N., Nogales E., Vulliamy T., Dokal I. Mutations in the telomere capping complex in bone marrow failure and related syndromes. Haematologica 2012, 97:524-528.
51. Wellinger R.J., Zakian V.A. Everything you ever wanted to know about Saccharomyces cerevisiae telomeres: beginning to end. Genetics 2012, 191:1073-1105.
52. Zubko M.K., Lydall D. Linear chromosome maintenance in the absence of essential telomere-capping proteins. Nat. Cell Biol. 2006, 8:734-740.
53. Zubko M.K., Guillard S., Lydall D. Exo1 and Rad24 differentially regulate generation of ssDNA at telomeres of Saccharomyces cerevisiae cdc13-1 mutants. Genetics 2004, 168:103-115.
54. Zubko M.K., Maringele L., Foster S.S., Lydall D. Detecting repair intermediates in vivo: effects of DNA damage response genes on single-stranded DNA accumulation at uncapped telomeres in budding yeast. Methods Enzymol. 2006, 409:285-300.