The roles of WRN and BLM RecQ helicases in the Alternative Lengthening of Telomeres

Nucleic Acids Research

Volumn 40, Issue 21, 2012, Pages 10809-10820

  Mendez Bermudez, Aaron ^a   Hidalgo Bravo, Alberto ^a   Cotton, Victoria E ^a   Gravani, Athanasia ^a   Jeyapalan, Jennie N ^a   Royle, Nicola J ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOM SYNDROME HELICASE; WERNER SYNDROME PROTEIN;

ARTICLE; CELL GROWTH; CELL LINE; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; HUMAN; HUMAN CELL; MUTATION; MUTATION RATE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; RNA INTERFERENCE; SISTER CHROMATID EXCHANGE; TELOMERE;

BASE SEQUENCE; CELL LINE; DOWN-REGULATION; EXODEOXYRIBONUCLEASES; HUMANS; MALE; MIDDLE AGED; MINISATELLITE REPEATS; MOLECULAR SEQUENCE DATA; MUTATION; RECQ HELICASES; TELOMERE; TELOMERE HOMEOSTASIS;

EID: 84870606493     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks862     Document Type: Article

References (71)

1. Chu, W.K. and Hickson, I.D. (2009) RecQ helicases: multifunctional genome caretakers. Nat. Rev. Cancer, 9, 644-654.
2. Chu, W.K., Hanada, K., Kanaar, R. and Hickson, I.D. (2010) BLM has early and late functions in homologous recombination repair in mouse embryonic stem cells. Oncogene, 29, 4705-4714.
3. Bohr, V.A. (2008) Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem. Sci., 33, 609-620.
4. 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. (Pubitemid 32685049)
5. 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.
6. Prince, P.R., Emond, M.J. and Monnat, R.J. Jr (2001) Loss of Werner syndrome protein function promotes aberrant mitotic recombination. Genes Dev., 15, 933-938. (Pubitemid 32323543)
7. Ouyang, K.J., Woo, L.L. and Ellis, N.A. (2008) Homologous recombination and maintenance of genome integrity: cancer and aging through the prism of human RecQ helicases. Mech Ageing Dev., 129, 425-440.
8. Hagelstrom, R.T., Blagoev, K.B., Niedernhofer, L.J., Goodwin, E.H. and Bailey, S.M. (2010) Hyper telomere recombination accelerates replicative senescence and may promote premature aging. Proc. Natl Acad. Sci. U.S.A., 107, 15768-15773.
9. Verdun, R.E. and Karlseder, J. (2007) Replication and protection of telomeres. Nature, 447, 924-931. (Pubitemid 46975759)
10. Gilson, E. and Geli, V. (2007) How telomeres are replicated. Nat. Rev. Mol. Cell. Biol., 8, 825-838. (Pubitemid 47462137)
11. Sfeir, A., Kosiyatrakul, S.T., Hockemeyer, D., MacRae, S.L., Karlseder, J., Schildkraut, C.L. and de Lange, T. (2009) Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell, 138, 90-103.
12. Crabbe, L., Verdun, R.E., Haggblom, C.I. and Karlseder, J. (2004) Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science, 306, 1951-1953. (Pubitemid 39627862)
13. Crabbe, L., Jauch, A., Naeger, C.M., Holtgreve-Grez, H. and Karlseder, J. (2007) Telomere dysfunction as a cause of genomic instability in Werner syndrome. Proc. Natl Acad. Sci. U.S.A., 104, 2205-2210. (Pubitemid 46391376)
14. Opresko, P.L., Otterlei, M., Graakjaer, J., Bruheim, P., Dawut, L., Kolvraa, S., May, A., Seidman, M.M. and Bohr, V.A. (2004) The Werner syndrome helicase and exonuclease cooperate to resolve telomeric D loops in a manner regulated by TRF1 and TRF2. Mol. Cell, 14, 763-774. (Pubitemid 38780850)
15. Laud, P.R., Multani, A.S., Bailey, S.M., Wu, L., Ma, J., Kingsley, C., Lebel, M., Pathak, S., DePinho, R.A. and Chang, S. (2005) Elevated telomere-telomere recombination in WRN-deficient, telomere dysfunctional cells promotes escape from senescence and engagement of the ALT pathway. Genes Dev., 19, 2560-2570. (Pubitemid 41565976)
16. Li, B., Jog, S.P., Reddy, S. and Comai, L. (2008) WRN controls formation of extrachromosomal telomeric circles and is required for TRF2DeltaB-mediated telomere shortening. Mol. Cell. Biol., 28, 1892-1904. (Pubitemid 351342621)
17. Schawalder, J., Paric, E. and Neff, N.F. (2003) Telomere and ribosomal DNA repeats are chromosomal targets of the bloom syndrome DNA helicase. B.M.C. Cell Biol., 4, 15.
18. Opresko, P.L., von Kobbe, C., Laine, J.P., Harrigan, J., Hickson, I.D. and Bohr, V.A. (2002) Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem., 277, 41110-41119. (Pubitemid 35215702)
19. Opresko, P.L., Mason, P.A., Podell, E.R., Lei, M., Hickson, I.D., Cech, T.R. and Bohr, V.A. (2005) POT1 stimulates RecQ helicases WRN and BLM to unwind telomeric DNA substrates. J. Biol. Chem., 280, 32069-32080. (Pubitemid 41361812)
20. Bai, Y. and Murnane, J.P. (2003) Telomere instability in a human tumor cell line expressing a dominant-negative WRN protein. Hum. Genet., 113, 337-347. (Pubitemid 37059116)
21. 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.
22. 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.
23. Varley, H., Pickett, H.A., Foxon, J.L., Reddel, R.R. and Royle, N.J. (2002) Molecular characterization of inter-telomere and intra-telomere mutations in human ALT cells. Nat. Genet., 30, 301-305.
24. Londono-Vallejo, J.A., Der-Sarkissian, H., Cazes, L., Bacchetti, S. and Reddel, R.R. (2004) Alternative lengthening of telomeres is characterized by high rates of telomeric exchange. Cancer Res., 64, 2324-2327. (Pubitemid 38523881)
25. Bailey, S.M., Brenneman, M.A. and Goodwin, E.H. (2004) Frequent recombination in telomeric DNA may extend the proliferative life of telomerase-negative cells. Nucleic Acids Res., 32, 3743-3751. (Pubitemid 39157721)
26. Murnane, J.P., Sabatier, L., Marder, B.A. and Morgan, W.F. (1994) Telomere dynamics in an immortal human cell-line. EMBO J., 13, 4953-4962. (Pubitemid 24319378)
27. Cesare, A.J. and Reddel, R.R. (2010) Alternative lengthening of telomeres: models, mechanisms and implications. Nat. Rev. Genet., 11, 319-330.
28. Henson, J.D. and Reddel, R.R. (2010) Assaying and investigating alternative lengthening of telomeres activity in human cells and cancers. FEBS Lett., 584, 3800-3811.
29. Monckton, D.G., Tamaki, K., MacLeod, A., Neil, D.L. and Jeffreys, A.J. (1993) Allele-specific MVR-PCR analysis at minisatellite D1S8. Hum. Mol. Genet., 2, 513-519. (Pubitemid 23140015)
30. Jeyapalan, J.N., Varley, H., Foxon, J.L., Pollock, R.E., Jeffreys, A.J., Henson, J.D., Reddel, R.R. and Royle, N.J. (2005) Activation of the ALT pathway for telomere maintenance can affect other sequences in the human genome. Hum. Mol. Genet., 14, 1785-1794. (Pubitemid 41418050)
31. Jeyapalan, J.N., Mendez-Bermudez, A., Zaffaroni, N., Dubrova, Y.E. and Royle, N.J. (2008) Evidence for alternative lengthening of telomeres in liposarcomas in the absence of ALT-associated PML bodies. Int. J. Cancer, 122, 2414-2421. (Pubitemid 351590472)
32. Cohen, H. and Sinclair, D.A. (2001) Recombination-mediated lengthening of terminal telomeric repeats requires the Sgs1 DNA helicase. Proc. Natl. Acad. Sci. U.S.A., 98, 3174-3179. (Pubitemid 32220818)
33. 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. (Pubitemid 32116846)
34. 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. (Pubitemid 29418720)
35. Lillard-Wetherell, K., Machwe, A., Langland, G.T., Combs, K.A., Behbehani, G.K., Schonberg, S.A., German, J., Turchi, J.J., Orren, D.K. and Groden, J. (2004) Association and regulation of the BLM helicase by the telomere proteins TRF1 and TRF2. Hum. Mol. Genet., 13, 1919-1932. (Pubitemid 39214340)
36. 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. (Pubitemid 35439426)
37. Fasching, C.L., Bower, K. and Reddel, R.R. (2005) Telomerase-independent telomere length maintenance in the absence of alternative lengthening of telomeres-associated promyelocytic leukemia bodies. Cancer Res., 65, 2722-2729. (Pubitemid 40490073)
38. Marciniak, R.A., Cavazos, D., Montellano, R., Chen, Q., Guarente, L. and Johnson, F.B. (2005) A novel telomere structure in a human alternative lengthening of telomeres cell line. Cancer Res., 65, 2730-2737. (Pubitemid 40490074)
39. Wu, L. and Hickson, I.D. (2002) The Bloom's syndrome helicase stimulates the activity of human topoisomerase IIIalpha. Nucleic Acids Res., 30, 4823-4829. (Pubitemid 35414641)
40. Wu, L. and Hickson, I.D. (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature, 426, 870-874. (Pubitemid 38056876)
41. Temime-Smaali, N., Guittat, L., Wenner, T., Bayart, E., Douarre, C., Gomez, D., Giraud-Panis, M.J., Londono-Vallejo, A., Gilson, E., Amor-Gueret, M. et al. (2008) Topoisomerase IIIalpha is required for normal proliferation and telomere stability in alternative lengthening of telomeres. EMBO. J., 27, 1513-1524. (Pubitemid 351733329)
42. Bhattacharyya, S., Keirsey, J., Russell, B., Kavecansky, J., Lillard-Wetherell, K., Tahmaseb, K., Turchi, J.J. and Groden, J. (2009) Telomerase-associated protein 1, HSP90, and topoisomerase IIalpha associate directly with the BLM helicase in immortalized cells using ALT and modulate its helicase activity using telomeric DNA substrates. J. Biol. Chem., 284, 14966-14977.
43. Huschtscha, L.I., Thompson, K.V. and Holliday, R. (1986) The susceptibility of Werner's syndrome and other human skin fibroblasts to SV40-induced transformation and immortalization. Proc. Roy. Soc. Lond. B. Biol. Sci., 229, 1-12. (Pubitemid 16010913)
44. Fukuchi, K., Martin, G.M. and Monnat, R.J. Jr (1989) Mutator phenotype of Werner syndrome is characterized by extensive deletions. Proc. Natl. Acad. Sci. U.S.A., 86, 5893-5897. (Pubitemid 19217554)
45. Baird, D.M., Jeffreys, A.J. and Royle, N.J. (1995) Mechanisms underlying telomere repeat turnover, revealed by hypervariable variant repeat distribution patterns in the human Xp/Yp telomere. EMBO J., 14, 5433-5443.
46. Mendez-Bermudez, A. and Royle, N.J. (2011) Deficiency in DNA mismatch repair increases the rate of telomere shortening in normal human cells. Hum. Mutat., 32, 939-946.
47. Baird, D.M., Coleman, J., Rosser, Z.H. and Royle, N.J. (2000) High levels of sequence polymorphism and linkage disequilibrium at the telomere of 12q: implications for telomere biology and human evolution. Am. J. Hum. Genet., 66, 235-250. (Pubitemid 30481486)
48. Jeffreys, A.J., Tamaki, K., MacLeod, A., Monckton, D.G., Neil, D.L. and Armour, J.A. (1994) Complex gene conversion events in germline mutation at human minisatellites. Nat. Genet., 6, 136-145. (Pubitemid 24188593)
49. Tamaki, K., Monckton, D.G., Macleod, A., Allen, M. and Jeffreys, A.J. (1993) 4-state MVR-PCR-increased discrimination of digital dna typing by simultaneous analysis of 2 polymorphic sites within minisatellite variant repeats at D1S8. Hum. Mol. Genet., 2, 1629-1632. (Pubitemid 23358681)
50. Berg, I., Neumann, R., Cederberg, H., Rannug, U. and Jeffreys, A.J. (2003) Two modes of germline instability at human minisatellite MS1 (locus D1S7): complex rearrangements and paradoxical hyperdeletion. Am. J. Hum. Genet., 72, 1436-1447. (Pubitemid 36628383)
51. Tamaki, K., May, C.A., Dubrova, Y.E. and Jeffreys, A.J. (1999) Extremely complex repeat shuffling during germline mutation at human minisatellite B6.7. Hum. Mol. Genet., 8, 879-888. (Pubitemid 29189056)
52. Coleman, J., Baird, D.M. and Royle, N.J. (1999) The plasticity of human telomeres demonstrated by a hypervariable telomere repeat array that is located on some copies of 16p and 16q. Hum. Mol. Genet., 8, 1637-1646. (Pubitemid 29423872)
53. Palm, W. and de Lange, T. (2008) How shelterin protects Mammalian telomeres. Annu. Rev. Genet., 42, 301-334.
54. Baird, D.M., Rowson, J., Wynford-Thomas, D. and Kipling, D. (2003) Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat. Genet., 33, 203-207. (Pubitemid 36177075)
55. Gaymes, T.J., North, P.S., Brady, N., Hickson, I.D., Mufti, G.J. and Rassool, F.V. (2002) Increased error-prone non homologous DNA end-joining-a proposed mechanism of chromosomal instability in Bloom's syndrome. Oncogene, 21, 2525-2533. (Pubitemid 34438105)
56. Wang, Y., Smith, K., Waldman, B.C. and Waldman, A.S. (2011) Depletion of the Bloom syndrome helicase stimulates homology-dependent repair at double-strand breaks in human chromosomes. DNA Repair, 10, 416-426.
57. Adams, M.D., McVey, M. and Sekelsky, J.J. (2003) Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science, 299, 265-267. (Pubitemid 36125215)
58. Lahkim Bennani-Belhaj, K., Rouzeau, S., Buhagiar-Labarchede, G., Chabosseau, P., Onclercq-Delic, R., Bayart, E., Cordelieres, F., Couturier, J. and Amor-Gueret, M. The Bloom syndrome protein limits the lethality associated with RAD51 deficiency. Mol. Cancer Res., 8, 385-394.
59. Jeffreys, A.J., Tamaki, K., Macleod, A., Monckton, D.G., Neil, D.L. and Armour, J. (1994) Complex gene conversion events in germline mutation at human minisatellites. Nat. Genet., 6, 136-145. (Pubitemid 24188593)
60. Jeffreys, A.J. and Neumann, R. (1997) Somatic mutation processes at a human minisatellite. Hum. Mol. Genet., 6, 129-136. (Pubitemid 27033976)
61. McVey, M., Adams, M., Staeva-Vieira, E. and Sekelsky, J.J. (2004) Evidence for multiple cycles of strand invasion during repair of double-strand gaps in Drosophila. Genetics, 167, 699-705. (Pubitemid 38931858)
62. McEachern, M.J. and Haber, J.E. (2006) Break-induced replication and recombinational telomere elongation in yeast. Annu. Rev. Biochem., 75, 111-135. (Pubitemid 44118028)
63. Royle, N.J., Mendez-Bermudez, A., Gravani, A., Novo, C., Foxon, J., Williams, J., Cotton, V. and Hidalgo, A. (2009) The role of recombination in telomere length maintenance. Biochem. Soc. Trans., 37, 589-595.
64. Lundblad, V. and Blackburn, E.H. (1993) An alternative pathway for yeast telomere maintenance rescues est1-senescence. Cell, 73, 347-360. (Pubitemid 23123312)
65. Siddiqa, A., Cavazos, D., Chavez, J., Long, L. and Marciniak, R.A. (2012) Modulation of telomeres in alternative lengthening of telomeres type I like human cells by the expression of werner protein and telomerase. J. Oncol., 2012, 806382.
66. Larocque, J.R. and Jasin, M. (2010) Mechanisms of recombination between diverged sequences in wild-type and BLM-deficient mouse and human cells. Mol. Cell. Biol., 30, 1887-1897.
67. LaRocque, J.R., Stark, J.M., Oh, J., Bojilova, E., Yusa, K., Horie, K., Takeda, J. and Jasin, M. (2011) Interhomolog recombination and loss of heterozygosity in wild-type and Bloom syndrome helicase (BLM)-deficient mammalian cells. Proc. Natl Acad. Sci. U.S.A., 108, 11971-11976.
68. Muntoni, A., Neumann, A.A., Hills, M. and Reddel, R.R. (2009) Telomere elongation involves intra-molecular DNA replication in cells utilizing alternative lengthening of telomeres. Hum. Mol. Genet., 18, 1017-1027.
69. Bhattacharyya, S., Sandy, A. and Groden, J. (2010) Unwinding protein complexes in ALTernative telomere maintenance. J. Cell. Biochem., 109, 7-15.
70. Jobling, M.A., Bouzekri, N. and Taylor, P.G. (1998) Hypervariable digital DNA codes for human paternal lineages: MVR-PCR at the Y-specific minisatellite, MSY1 (DYF155S1). Hum. Mol. Genet., 7, 643-653. (Pubitemid 28152263)
71. Shanks, M.E., May, C.A., Dubrova, Y.E., Balaresque, P., Rosser, Z.H., Adams, S.M. and Jobling, M.A. (2008) Complex germline and somatic mutation processes at a haploid human minisatellite shown by single-molecule analysis. Mutat. Res., 648, 46-53.