Replication protein A prevents accumulation of single-stranded telomeric DNA in cells that use alternative lengthening of telomeres

Nucleic Acids Research

Volumn 35, Issue 21, 2007, Pages 7267-7278

  Grudic, Amra ^a,b   Jul Larsen, Åsne ^a,b   Haring, Stuart J ^c   Wold, Marc S ^c   Lønning, Per Eystein ^a   Bjerkvig, Rolf ^b,d   Bøe, Stig Ove ^a,b  

^a HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF BERGEN   (Norway)

^c UNIVERSITY OF IOWA   (United States)

^d NorLux Neuro Oncology   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; PROTEIN A; SINGLE STRANDED DNA; TELOMERASE;

ALTERNATIVE RNA SPLICING; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CHROMOSOME SIZE; DNA REPLICATION; HUMAN; HUMAN CELL; METAPHASE CHROMOSOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; TELOMERE;

CELL CYCLE; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; DNA, SINGLE-STRANDED; HUMANS; NEOPLASMS; REPLICATION PROTEIN A; RNA INTERFERENCE; TELOMERE;

EID: 37549060645     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm738     Document Type: Article

References (42)

1. Smogorzewska,A. and de Lange,T. (2004) Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem., 73, 177-208.
2. Henson,J.D., Neumann,A.A., Yeager,T.R. and Reddel,R.R. (2002) Alternative lengthening of telomeres in mammalian cells. Oncogene, 21, 598-610.
3. Cesare,A.J. and Griffith,J.D. (2004) Telomeric: DNA in ALT cells is characterized by free telomeric circles and heterogeneous t-loops. Mol. Cell. Biol., 24, 9948-9957.
4. Natarajan,S. and McEachem,M.J. (2002) Recombinational telomere elongation promoted by DNA circles. Mol. Cell. Biol., 22, 4512-4521.
5. Wang,R.C., Smogorzewska,A. and de Lange,T. (2004) Homologous recombination generates T-loop-sized deletions at human telomeres. Cell, 119, 355-368.
6. Compton,S.A., Choi,J.H., Cesare,A.J., Ozgur,S. and Griffith,J.D. (2007) Xrcc3 and Nbs1 are required for the production of extrachromosomal telomeric circles in human alternative lengthening of telomere cells. Cancer Res., 67, 1513-1519.
7. Yeager,T.R., Neumann,A.A., Englezou,A., Huschtscha,L.I., Noble,J.R. and Reddel,R.R. (1999) Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res., 59, 4175-4179.
8. Fasching,C.L., Neumann,A.A., Muntoni,A., Yeager,T.R. and Reddel,R.R. (2007) DNA damage induces alternative lengthening of telomeres (ALT) associated promyelocytic leukemia bodies that preferentially associate with linear telomeric DNA. Cancer Res., 67, 7072-7077.
9. Binz,S.K., Sheehan,A.M. and Wold,M.S. (2004) Replication protein A phosphorylation and the cellular response to DNA damage. DNA Repair (Amst.), 3, 1015-1024.
10. Wold,M.S. (1997) Replication protein A: A heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem., 66, 61-92.
11. Croy,J.E. and Wuttke,D.S. (2006) Themes in ssDNA recognition by telomere-end protection proteins. Trends Biochem. Sci., 31, 516-525.
12. Gao,H., Cervantes,R.B., Mandell,E.K., Otero,J.H. and Lundblad,V. (2007) RPA-like proteins mediate yeast telomere function. Nat. Struct. Mol. Biol., 14, 208-214.
13. Salas,T.R., Petruseva,I., Lavrik,O., Bourdoncle,A., Mergny,J.L., Favre,A. and Saintome,C. (2006) Human replication protein A unfolds telomeric G-quadruplexes. Nucleic Acids Res., 34, 4857-4865.
14. Zang,A.J., Podell,E.R. and Cech,T.R. (2005) Human POT1 disrupts telomeric G-quadruplexes allowing telomerase extension in vitro. Proc. Natl Acad. Sci. USA, 102, 10864-40869.
15. Schramke,V., Luciano,P., Brevet,V., Guillot,S., Corda,Y., Longhese,M.P., Gilson,E. and Geli,V. (2004) RPA regulates telomerase action by providing Estlp access to chromosome ends. Nat. Genet., 36, 46-54.
16. Chandra,A., Hughes,T.R., Nugent,C.I. and Lundblad,V. (2001) Cdc13 both positively and negatively regulates telomere replication. Genes Dev. 15, 404-414.
17. Colgin,L.M., Baran,K., Baumann,P., Cech,T.R. and Reddel,R.R. (2003) Human POT1 facilitates telomere elongation by telomerase. Curr. Biol. 13, 942-946.
18. Evans,S.K. and Lundblad,V. (1999) Est1 and Cdc13 as comediators of telomerase access. Science, 286, 117-120.
19. Froelich-Ammon,S.J., Dickinson,B.A., Bevilacqua,J.M., Schultz,S.C. and Cech,T.R. (1998) Modulation of telomerase activity by telomere DNA-binding proteins in Oxytricha. Genes Dev., 12, 1504-1514.
20. Loayza,D. and De Lange,T. (2003) POT1 as a terminal transducer of TRF1 telomere length control. Nature, 423, 1013-1018.
21. Kibe,T., Ono,Y., Sato,K. and Ueno,M. (2007) Fission yeast Taz1 and RPA are synergistically required to prevent rapid telomere loss. Mol. Biol. Cell, 18, 2378-2387.
22. Smith,J., Zou,H. and Rothstein,R. (2000) Characterization of genetic interactions with RFA1: The role of RPA in DNA replication and telomere maintenance. Biochimie, 82, 71-78.
23. Larrivee,M. and Wellinger,R.J. (2006) Telomerase- and capping-independent yeast survivors with alternate telomere states. Nat. Cell Biol., 8, 741-747.
24. Petreaca,R.C. Chiu,H.C., Eckelhoefer,H.A., Chuang,C., Xu,L. and Nugent,C.I. (2006) Chromosome end protection plasticity revealed by Stn1p and Ten1p bypass of Cdc13p. Nat. Cell Biol., 8, 748-755.
25. Zubko,M.K. and Lydall,D. (2006) Linear chromosome maintenance in the absence of essential telomere-capping proteins. Nat. Cell Biol., 8, 734-740.
26. Boe,S.O., Haave,M., Jul-Larsen,A., Grudic,A., Bjerkvig,R. and Lonning,P.E. (2006) Promyelocytic leukemia nuclear bodies are predetermined processing sites for damaged DNA. J. Cell Sci., 119, 3284-3295.
27. Jul-Larsen,A., Visted,T., Karlsen,B.O., Rinaldo,C.H., Bjerkvig,R., Lonning,P.E. and Boe,S.O. (2004) PML-nuclear bodies accumulate DNA in response to polyomavirus BK and simian virus 40 replication. Exp. Cell Res., 298, 58-73.
28. Kenny,M.K., Schlegel,U., Furneaux,H. and Hurwitz,J. (1990) The role of human single-stranded DNA binding protein and its individual subunits in simian virus 40 DNA replication. J. Biol. Chem., 265, 7693-7700.
29. Leej,J.J., Warburton,D. and Robertson,E.J. (1990) Cytogenetic methods for the mouse: Preparation of chromosomes, karyotyping, and in situ hybridization. Anal. Biochem., 189, 1-17.
30. Zijlmans,J.M., Martens,U.M., Poon,S.S., Raap,A.K., Tanke,H.J., Ward,R.K. and Lansdorp,P.M. (1997) Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats. Proc. Natl Acad. Sci. USA, 94, 7423-7428.
31. Karlseder,J., Smogorzewska,A. and de Lange,T. (2002) Senescence induced by altered telomere state, not telomere loss. Science, 295, 2446-2449.
32. Brewer,B.J. and Fangman,W.L. (1987) The localization of replication origins on ARS plasmids in S. cerevisiae. Cell, 51, 463-471.
33. Dodson,G.E., Shi,Y. and Tibbetts,R.S. (2004) DNA replication defects, spontaneous DNA damage, and ATM-dependent checkpoint activation in replication protein A-deficient cells. J. Biol. Chem., 279, 34010-34014.
34. Churikov,D., Wei,C. and Price,C.M. (2006) Vertebrate POT1 restricts G-overhang length and prevents activation of a telomeric DNA damage checkpoint but is dispensable for overhang protection. Mol. Cell. Biol., 26, 6971-6982.
35. Garvik,B., Carson,M. and Hartwell,L. (1995) Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol. Cell. Biol., 15, 6128-6138.
36. Araya,R., Hirai,I., Meyerkord,C.L. and Wang,H.G. (2005) Loss of RPA1 induces Chk2 phosphorylation through a caffeine-sensitive pathway. FEBS Lett., 579, 157-161.
37. Weinert,T.A. and Hartwell,L.H. (1993) Cell cycle arrest of cdc mutants and specificity of the RAD9 checkpoint. Genetics, 134, 63-80.
38. Lin,C.Y., Chang,H.H., Wu,K.J., Tseng,S.F., Lin,C.C., Lin,C.P. and Teng,S.C. (2005) Extrachromosomal telomeric circles contribute to Rad52-, Rad.50-, and polymerase delta-mediated telomere-telomere recombination in Saccharomyces cerevisiae. Eukaryot. Cell, 4 327-336.
39. Tomaska,L., McEachern,M.J. and Nosek,J. (2004) Alternatives to telomerase: Keeping linear chromosomes via telomeric circles. FEBS Lett., 567, 142-146.
40. Tomaska,L., Nosek,J., Makhov,A.M., Pastorakova,A. and Griffith,J.D. (2000) Extragenomic double-stranded DNA circles in yeast with linear mitochondrial genomes: Potential involvement in telomere maintenance. Nucleic Acids Res., 28, 4479-4487.
41. Smith,J. and Rothstein,R. (1995) A mutation in the gene encoding the Saccharomyces cerevisiae single-stranded DNA-binding protein Rfa1 stimulates a RAD52-independent pathway for direct-repeat recombination. Mol. Cell. Biol., 15, 1632-1641.
42. Stavropoulos,D.J., Bradshaw,P.S., Li,X., Pasic,I., Truong,K., Ikura,M., Ungrin,M. and Meyn,M.S. (2002) The Bloom syndrome helicase BLM interacts with TRF2 in ALT cells and promotes telomeric DNA synthesis. Hum. Mol. Genet., 11, 3135-3144.