The bloom syndrome helicase BLM interacts with TRF2 in ALT cells and promotes telomeric DNA synthesis

Human Molecular Genetics

Volumn 11, Issue 25, 2002, Pages 3135-3144

  Stavropoulos, Dimitrios J ^a,b   Bradshaw, Paul S ^a,b   Li, Xiaobin ^b   Pasic, Ivan ^a,b   Truong, Kevin ^c,d   Ikura, Mitsuhiko ^c,d   Ungrin, Mark ^c   Meyn, M Stephen ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GREEN FLUORESCENT PROTEIN; HELICASE; PROTEIN BLM; TELOMERIC REPEAT BINDING FACTOR 2; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; BLOOM SYNDROME PROTEIN; DNA; PHOTOPROTEIN; RECOMBINANT PROTEIN;

BLOOM SYNDROME; CONTROLLED STUDY; DNA CONTENT; DNA SYNTHESIS; ENERGY TRANSFER; GENE OVEREXPRESSION; GENETIC RECOMBINATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; TELOMERE; ARTICLE; BIOSYNTHESIS; CELL LINE; CELL NUCLEUS; CHEMISTRY; ENZYMOLOGY; FIBROBLAST; GENETICS; IMMUNOLOGY; METABOLISM; VIROLOGY;

ADENOSINE TRIPHOSPHATASES; BLOOM SYNDROME; CELL LINE; CELL LINE, TRANSFORMED; CELL NUCLEUS; DNA; DNA HELICASES; FIBROBLASTS; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; RECOMBINANT PROTEINS; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 2;

EID: 0036899106     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/11.25.3135     Document Type: Review

References (59)

1. Counter, C.M., Avilion, A.A., LeFeuvre, C.E., Stewart, N.G., Greider, C.W, Harley, C.B. and Bacchetti, S. (1992) Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO. J, 11, 1921-1929.
2. Kim, N.W., Piatyszek, M.A., Prowse, K.R., Harley, C.B., West, M.D., Ho, P.L., Coviello, G.M., Wright, WE., Weinrich, S.L. and Shay, J.W. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science, 266, 2011-2015.
3. Counter, C.M., Hirte, H.W, Bacchetti, S. and Harley, C.B. (1994) Telomerase activity in human ovarian carcinoma. Proc. Natl Acad. Sci. USA, 91, 2900-2904.
4. Murnane, J.P., Sabatier, L., Marder, B.A. and Morgan, WF. (1994) Telomere dynamics in an immortal human cell line. EMBO. J., 13, 4953-4962.
5. Bryan, T.M., Englezou, A., Gupta, J., Bacchetti, S. and Reddel, R.R. (1995) Telomere elongation in immortal human cells without detectable telomerase activity. EMBO. J., 14, 4240-4248.
6. Bryan, T.M., Englezou, A., Dalla-Pozza, L., Dunham, M.A. and Reddel, R.R. (1997) Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med., 3, 1271-1274.
7. Bryan, T.M., Marusic, L., Bacchetti, S., Namba, M. and Reddel, R.R. (1997) The telomere lengthening mechanism in telomerase-negative immortal human cells does not involve the telomerase RNA subunit. Hum. Mol. Genet., 6, 921-926.
8. Ogino, H., Nakabayashi, K., Suzuki, M., Takahashi, E., Fujii, M., Suzuki, T. and Ayusawa, D. (1998) Release of telomeric DNA from chromosomes in immortal human cells lacking telomerase activity. Biochem. Biophys. Res. Commun., 248, 223-227.
9. Regev, A., Cohen, S., Cohen, E., Bar-Am, I. and Lavi, S. (1998) Telomeric repeats on small polydisperse circular DNA (spcDNA) and genomic instability. Oncogene, 17, 3455-3461.
10. Tokutake, Y., Matsumoto, T., Watanabe, T., Maeda, S., Tahara, H., Sakamoto, S., Niida, H., Sugimoto, M., Ide, T. and Furuichi, Y. (1998) Extra-chromosomal telomere repeat DNA in telomerase-negative immortalized cell lines. Biochem. Biophys. Res. Commun., 247, 765-772.
11. Lundblad, V. and Blackburn, E.H. (1993) An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell, 73, 347-360.
12. Friedberg, E.C. (1988) Deoxyribonucleic acid repair in the yeast Saccharomyces cerevisiae. Microbiol. Rev., 52, 70-102.
13. Le, S., Moore, J.K., Haber, J.E. and Greider, C.W (1999) RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics, 152, 143-152.
14. Teng, S.C. and Zakian, V.A. (1999) Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol. Cell. Biol., 19, 8083-8093.
15. 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.
16. Wu, G., Lee, W.H. and Chen, P.L. (2000) NBS1 and TRF1 colocalize at promyelocytic leukemia bodies during late S/G2 phases in immortalized telomerase-negative cells. Implication of NBS1 in alternative lengthening of telomeres. J. Biol. Chem., 275, 30618-30622.
17. Seeler, J.S. and Dejean, A. (1999) The PML nuclear bodies: actors or extras? Curr. Opin. Genet. Devl., 9, 362-367.
18. Quignon, F., De Bels, F., Koken, M., Feunteun, J., Ameisen, J.C. and de The, H. (1998) PML induces a novel caspase-independent death process. Nat. Genet., 20, 259-265.
19. Wang, Z.G., Ruggero, D., Ronchetti, S., Zhong, S., Gaboli, M., Rivi, R. and Pandolfi, P.P. (1998) PML is essential for multiple apoptotic pathways. Nat. Genet., 20, 266-272.
20. Wang, Z.G., Delva, L., Gaboli, M., Rivi, R., Giorgio, M., Cordon-Cardo, C., Grosveld, F. and Pandolfi, P.P. (1998) Role of PML in cell growth and the retinoic acid pathway. Science, 279, 1547-1551.
21. Zhong, S., Hu, P., Ye, T.Z., Stan, R., Ellis, N.A. and Pandolfi, P.P. (1999) A role for PML and the nuclear body in genomic stability. Oncogene, 18, 7941-7947.
22. Carbone, R., Pearson, M., Minucci, S. and Pelicci, PG. (2002) PML NBs associate with the hMre11 complex and p53 at sites of irradiation induced DNA damage. Oncogene, 21, 1633-1640.
23. Bischof, O., Kim, S.H., Irving, J., Beresten, S., Ellis, N.A. and Campisi, J. (2001) Regulation and localization of the Bloom syndrome protein in response to DNA damage. J. Cell. Biol., 153, 367-380.
24. Dunham, M.A., Neumann, A.A., Fasching, C.L. and Reddel, R.R. (2000) Telomere maintenance by recombination in human cells. Nat. Genet., 26, 447-450.
25. Ellis, N.A., Groden, J., Ye, T.Z., Straughen, J., Lennon, D.J., Ciocci, S., Proytcheva, M. and German, J. (1995) The Bloom's syndrome gene product is homologous to RecQ helicases. Cell, 83, 655-666.
26. Johnson, F.B., Lombard, D.B., Neff, N.F., Mastrangelo, M.A., Dewolf, W., Ellis, N.A., Marciniak, R.A., Yin, Y., Jaenisch, R. and Guarente, L. (2000) Association of the Bloom syndrome protein with topoisomerase IIIalpha in somatic and meiotic cells, Cancer Res., 60, 1162-1167.
27. van Brabant, A.J., Ye, T., Sanz, M., German, I.J., Ellis, N.A. and Holloman, W.K. (2000) Binding and melting of D-loops by the Bloom syndrome helicase. Biochemistry, 39, 14617-14625.
28. Wa, L., Davies, S.L., Levitt, N.C. and Hickson, I.D. (2001) Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J. Biol. Chem., 276, 19375-19381.
29. Walpita, D., Plug, A.W., Neff, N.F., German, J. and Ashley, T. (1999) Bloom's syndrome protein, BLM, colocalizes with replication protein A in meiotic prophase nuclei of mammalian spermatocytes. Proc. Natl Acad. Sci. USA, 96, 5622-5627.
30. Karow, J.K., Constantinou, A., Li, J.L., West, S.C. and Hickson, I.D. (2000) The Bloom's syndrome gene product promotes branch migration of holiday junctions. Proc. Natl Acad. Sci. USA, 97, 6504-6508.
31. Sun, H., Karow, J.K., Hickson, I.D. and Maizels, N. (1998) The Bloom's syndrome helicase unwinds G4 DNA. J. Biol. Chem., 273, 27587-27592.
32. German, J. (1993) Bloom syndrome: a mendelian prototype of somatic mutational disease. Medicine (Baltimore), 72, 393-406.
33. Yankiwski, V, Marciniak, R.A., Guarente, L. and Neff, N.F. (2000) Nuclear structure in normal and Bloom syndrome cells. Proc. Natl Acad. Sci. USA, 97, 5214-5219.
34. Ishov, A.M., Sotnikov, A.G., Negorev, D., Vladimirova, O.V., Neff, N., Kamitani, T., Yeh, E.T., Strauss, J.F., III and Maul, G.G. (1999) PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J Cell. Biol., 147, 221-234.
35. Neff, N.F., Ellis, N.A., Ye, T.Z., Noonan, J., Huang, K., Sanz, M. and Proytcheva, M. (1999) The DNA helicase activity of BLM is necessary for the correction of the genomic instability of bloom syndrome cells. Mol. Biol. Cell, 10, 665-676.
36. Miyawaki, A. and Tsien, R.Y. (2000) Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Meth. Enzymol., 327, 472-500.
37. Grobelny, J.V., Kalp-McEliece, M. and Broccoli, D. (2001) Effects of reconstitution of telomerase activity on telomere maintenance by the alternative lengthening of telomeres (ALT) pathway. Hum. Mol. Genet., 10, 1953-1961.
38. Cerone, M.A., Londono-Vallejo, J.A. and Bacchetti, S. (2001) Telomere maintenance by telomerase and by recombination can coexist in human cells. Hum. Mol. Genet., 10, 1945-1952.
39. van Steensel, B., Smogorzewska, A. and de Lange, T. (1998) TRF2 protects human telomeres from end-to-end fusions. Cell, 92, 401-413.
40. Griffith, J.D., Comeau, L., Rosenfield, S., Stansel, R.M., Bianchi, A., Moss, H. and de Lange, T. (1999) Mammalian telomeres end in a large duplex loop. Cell, 97, 503-514.
41. Karlseder, J., Broccoli, D., Dai, Y., Hardy, S. and de Lange, T. (1999) p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science, 283, 1321-1325.
42. Perrem, K., Bryan, T.M., Englezou, A., Hackl, T., Moy, E.L. and Reddel, R.R. (1999) Repression of an alternative mechanism for lengthening of telomeres in somatic cell hybrids. Oncogene, 18, 3383-3390.
43. Huang, P., Pryde, F.E., Lester, D., Maddison, R.L., Borts, R.H., Hickson, I.D. and Louis, E.J. (2001) SGS1 is required for telomere elongation in the absence of telomerase. Curr. Biol., 11, 125-129.
44. Johnson, F.B., Marciniak, R.A., McVey, M., Stewart, S.A., Hahn, W.C. and Guarente, L. (2001) The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO. J., 20, 905-913.
45. Cohen, H. and Sinclair, D.A. (2001) Recombination-mediated lengthening of terminal telomeric repeats requires the Sgs1 DNA helicase. Proc. Natl Acad. Sci. USA, 98, 3174-3179.
46. Teng, S.C., Chang, J., McCowan, B. and Zakian, VA. (2000) Telomerase-independent lengthening of yeast telomeres occurs by an abrupt Rad50p-dependent, Rif-inhibited recombinational process. Mol. Cell., 6, 947-952.
47. Bosco, G. and Haber, J.E. (1998) Chromosome break-induced DNA replication leads to nonreciprocal translocations and telomere capture. Genetics, 150, 1037-1047.
48. Natarajan, S. and McEachern, M.J. (2002) Recombinational telomere elongation promoted by DNA circles. Mol. Cell. Biol., 22, 4512-4521.
49. Harmon, F.G. and Kowalczykowski, S.C. (1998) RecQ helicase, in concert with RecA and SSB proteins, initiates and disrupts DNA recombination. Genes. Devl., 12, 1134-1144.
50. Karow, J.K., Chakraverty, R.K. and Hickson, I.D. (1997) The Bloom's syndrome gene product is a 3′-5′ DNA helicase. J. Biol. Chem., 272, 30611-30614.
51. Mohaghegh, P., Karow, J.K., Brosh, R.M., Jr., Bohr, V.A. and Hickson, I.D. (2001) The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res., 29, 2843-2849.
52. Hu, P., Beresten, S.F., van Brabant, A.J., Ye, T.Z., Pandolfi, P.P., Johnson, F.B., Guarente, L. and Ellis, N.A. (2001) Evidence for BLM and topoisomerase III alpha interaction in genomic stability. Hum. Mol. Genet., 10, 1287-1298.
53. Sambrook, J., F.E.F.a.M.T. (1989) Molecular Cloning: a Laboratory Manual., 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
54. van Steensel, B. and de lange, T. (1997) Control of telomere length by the human telomeric protein TRF1. Nature, 385, 740-743.
55. Zhu, X.D., Kuster, B., Mann, M., Petrim, J.H. and Lange, T. (2000) Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet., 25, 347-352.
56. Gharibyan, V and Youssoufian, H. (1999) Localization of the Bloom syndrome helicase to punctate nuclear structures and the nuclear matrix and regulation during the cell cycle: comparison with the Werner's syndrome helicase. Mol. Carcinog., 26, 261-273.
57. Wu, L., Davies, S.L., North, P.S., Goulaouic, H., Riou, J.F., Turley, H., Gatter, K.C. and Hickson, I.D. (2000) The Bloom's syndrome gene product interacts with topoisomerase III. J. Biol. Chem., 275, 9636-9644.
58. Rufer, N., Dragowska, W., Thornbury, G., Roosnek, E. and Lansdorp, P.M. (1998) Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry. Nat. Biotechnol., 16, 743-747.
59. 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.