The werner syndrome helicase and exonuclease cooperate to resolve telomeric D loops in a manner regulated by TRF1 and TRF2

Molecular Cell

Volumn 14, Issue 6, 2004, Pages 763-774

  Opresko, Patricia L ^a   Otterlei, Marit ^b   Graakjær, Jesper ^c   Bruheim, Per ^b   Dawut, Lale ^a   Kølvraa, Steen ^c   May, Alfred ^a   Seidman, Michael M ^a   Bohr, Vilhem A ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DNA; EXONUCLEASE; HELICASE; PROTIRELIN 1; PROTIRELIN 2; PROTIRELIN DERIVATIVE; TELOMERASE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE S PHASE; CONTROLLED STUDY; DISSOCIATION; ENZYME ACTIVITY; EROSION; FIBROBLAST; GENE REPLICATION; GENE STRUCTURE; GENETIC RECOMBINATION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; PREMATURE AGING; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SENESCENCE; TELOMERE; WERNER SYNDROME; YEAST;

CELL LINE, TUMOR; DNA HELICASES; EXONUCLEASES; HELA CELLS; HUMANS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN STRUCTURE, TERTIARY; RECQ HELICASES; S PHASE; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 1; TELOMERIC REPEAT BINDING PROTEIN 2;

EID: 2942637828     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2004.05.023     Document Type: Article

References (43)

1. Bai Y., Murnane J.P. Telomere instability in a human tumor cell line expressing a dominant-negative WRN protein. Hum. Genet. 113:2003;337-347
2. Baynton K., Otterlei M., Bjoras M., von Kobbe C., Bohr V.A., Seeberg E. WRN interacts physically and functionally with the recombination mediator protein RAD52. J. Biol. Chem. 278:2003;36476-36486
3. Blackburn E.H. Telomere states and cell fates. Nature. 408:2000;53-56
4. Bodnar A.G., Ouellette M., Frolkis M., Holt S.E., Chiu C.P., Morin G.B., Harley C.B., Shay J.W., Lichtsteiner S., Wright W.E. Extension of life-span by introduction of telomerase into normal human cells. Science. 279:1998;349-352
5. Broccoli D., Smogorzewska A., Chong L., De Lange T. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat. Genet. 17:1997;231-235
6. Chen L., Huang S., Lee L., Davalos A., Schiestl R.H., Campisi J., Oshima J. WRN, the protein deficient in Werner syndrome, plays a critical structural role in optimizing DNA repair. Aging Cell. 2:2003;191-199
7. Cohen H., Sinclair D.A. Recombination-mediated lengthening of terminal telomeric repeats requires the Sgs1 DNA helicase. Proc. Natl. Acad. Sci. USA. 98:2001;3174-3179
8. Constantinou A., Tarsounas M., Karow J.K., Brosh R.M., Bohr V.A., Hickson I.D., West S.C. Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep. 1:2000;80-84
9. Davis T., Singhrao S.K., Wyllie F.S., Haughton M.F., Smith P.J., Wiltshire M., Wynford-Thomas D., Jones C.J., Faragher R.G., Kipling D. Telomere-based proliferative lifespan barriers in Werner-syndrome fibroblasts involve both p53-dependent and p53-independent mechanisms. J. Cell Sci. 116:2003;1349-1357
10. De Lange T. Protection of mammalian telomeres. Oncogene. 21:2002;532-540
11. Dunham M.A., Neumann A.A., Fasching C.L., Reddel R.R. Telomere maintenance by recombination in human cells. Nat. Genet. 26:2000;447-450
12. Griffith J.D., Comeau L., Rosenfield S., Stansel R.M., Bianchi A., Moss H., De Lange T. Mammalian telomeres end in a large duplex loop. Cell. 97:1999;503-514
13. Grigorova M., Balajee A.S., Natarajan A.T. Spontaneous and X-ray-induced chromosomal aberrations in Werner syndrome cells detected by FISH using chromosome-specific painting probes. Mutagenesis. 15:2000;303-310
14. Henson J.D., Neumann A.A., Yeager T.R., Reddel R.R. Alternative lengthening of telomeres in mammalian cells. Oncogene. 21:2002;598-610
15. Hickson I.D. RecQ helicases. caretakers of the genome Nat. Rev. Cancer. 3:2003;169-178
16. Huang S., Li B., Gray M.D., Oshima J., Mian I.S., Campisi J. The premature ageing syndrome protein, WRN, is a 3′→5′ exonuclease. Nat. Genet. 20:1998;114-116
17. Huang P., Pryde F.E., Lester D., Maddison R.L., Borts R.H., Hickson I.D., Louis E.J. SGS1 is required for telomere elongation in the absence of telomerase. Curr. Biol. 11:2001;125-129
18. Johnson F.B., Marciniak R.A., McVey M., Stewart S.A., Hahn W.C., Guarente L. The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO J. 20:2001;905-913
19. Karlseder J., Broccoli D., Dai Y., Hardy S., De Lange T. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science. 283:1999;1321-1325
20. Karlseder J., Smogorzewska A., De Lange T. Senescence induced by altered telomere state, not telomere loss. Science. 295:2002;2446-2449
21. Leonhardt H., Rahn H.P., Weinzierl P., Sporbert A., Cremer T., Zink D., Cardoso M.C. Dynamics of DNA replication factories in living cells. J. Cell Biol. 149:2000;271-280
22. Machwe A., Xiao L., Orren D.K. TRF2 recruits the Werner syndrome (WRN) exonuclease for processing of telomeric DNA. Oncogene. 23:2004;149-156
23. Martin G.M. Genetic syndromes in man with potential relevance to the pathobiology of aging. Birth Defects Orig. Artic. Ser. 14:1978;5-39
24. Mohaghegh P., Karow J.K., Brosh J.R. Jr., Bohr V.A., Hickson I.D. The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res. 29:2001;2843-2849
25. Opresko P.L., Laine J.P., Brosh R.M. Jr., Seidman M.M., Bohr V.A. Coordinate action of the helicase and 3′ to 5′ exonuclease of Werner syndrome protein. J. Biol. Chem. 276:2001;44677-44687
26. Opresko P.L., von Kobbe C., Laine J.P., Harrigan J., Hickson I.D., Bohr V.A. Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem. 277:2002;41110-41119
27. Opresko P.L., Cheng W.H., von Kobbe C., Harrigan J.A., Bohr V.A. Werner syndrome and the function of the Werner protein; what they can teach us about the molecular aging process. Carcinogenesis. 24:2003;791-802
28. Orren D.K., Theodore S., Machwe A. The Werner syndrome helicase/exonuclease (WRN) disrupts and degrades D-loops in vitro. Biochemistry. 41:2002;13483-13488
29. Prince P.R., Emond M.J., Monnat R.J. Jr. Loss of Werner syndrome protein function promotes aberrant mitotic recombination. Genes Dev. 15:2001;933-938
30. Saintigny Y., Makienko K., Swanson C., Emond M.J., Monnat J.R. Jr. Homologous recombination resolution defect in werner syndrome. Mol. Cell. Biol. 22:2002;6971-6978
31. Salk D., Au K., Hoehn H., Martin G.M. Cytogenetic aspects of Werner syndrome. Adv. Exp. Med. Biol. 190:1985;541-546
32. Schulz V.P., Zakian V.A., Ogburn C.E., McKay J., Jarzebowicz A.A., Edland S.D., Martin G.M. Accelerated loss of telomeric repeats may not explain accelerated replicative decline of Werner syndrome cells. Hum. Genet. 97:1996;750-754
33. Stavropoulos D.J., Bradshaw P.S., Li X., Pasic I., Truong K., Ikura M., Ungrin M., Meyn M.S. The Bloom syndrome helicase BLM interacts with TRF2 in ALT cells and promotes telomeric DNA synthesis. Hum. Mol. Genet. 11:2002;3135-3144
34. Stefanini M., Scappaticci S., Lagomarsini P., Borroni G., Berardesca E., Nuzzo F. Chromosome instability in lymphocytes from a patient with Werner's syndrome is not associated with DNA repair defects. Mutat. Res. 219:1989;179-185
35. Tahara H., Tokutake Y., Maeda S., Kataoka H., Watanabe T., Satoh M., Matsumoto T., Sugawara M., Ide T., Goto M., et al. Abnormal telomere dynamics of B-lymphoblastoid cell strains from Werner's syndrome patients transformed by Epstein-Barr virus. Oncogene. 15:1997;1911-1920
36. van Steensel B., Smogorzewska A., De Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell. 92:1998;401-413
37. von Kobbe C., Thoma N.H., Czyzewski B.K., Pavletich N.P., Bohr V.A. Werner syndrome protein contains three structure-specific DNA binding domains. J. Biol. Chem. 278:2003;52997-53006
38. Wu G., Lee W.H., Chen P.L. NBS1 and TRF1 colocalize at PML bodies during late S/G2 phases in immortalized telomerase-negative cells. Implication of NBS1 in alternative lengthening of telomeres. J. Biol. Chem. 275:2000;30618-30622
39. Wu G., Jiang X., Lee W.H., Chen P.L. Assembly of functional ALT-associated promyelocytic leukemia bodies requires Nijmegen Breakage Syndrome 1. Cancer Res. 63:2003;2589-2595
40. Wyllie F.S., Jones C.J., Skinner J.W., Haughton M.F., Wallis C., Wynford-Thomas D., Faragher R.G., Kipling D. Telomerase prevents the accelerated cell ageing of Werner syndrome fibroblasts. Nat. Genet. 24:2000;16-17
41. Yankiwski V., Marciniak R.A., Guarente L., Neff N.F. Nuclear structure in normal and Bloom syndrome cells. Proc. Natl. Acad. Sci. USA. 97:2000;5214-5219
42. Yeager T.R., Neumann A.A., Englezou A., Huschtscha L.I., Noble J.R., Reddel R.R. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59:1999;4175-4179
43. Yu C.E., Oshima J., Fu Y.H., Wijsman E.M., Hisama F., Alisch R., Matthews S., Nakura J., Miki T., Ouais S., et al. Positional cloning of the Werner's syndrome gene. Science. 272:1996;258-262