Variant repeats are interspersed throughout the telomeres and recruit nuclear receptors in ALT cells

Journal of Cell Biology

Volumn 199, Issue 6, 2012, Pages 893-906

  Conomos, Dimitri ^a,b   Stutz, Michael D ^a,b   Hills, Mark ^c   Neumann, Axel A ^a,b   Bryan, Tracy M ^a,b   Reddel, Roger R ^a,b   Pickett, Hilda A ^a,b  

^a CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c BRITISH COLUMBIA CANCER AGENCY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; TELOMERASE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CHROMOSOME VARIANT; DNA CONTENT; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC RECOMBINATION; INTERSPERSED REPEAT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TELOMERE HOMEOSTASIS;

BASE SEQUENCE; BINDING SITES; CELL LINE; COUP TRANSCRIPTION FACTOR II; HUMANS; MUTATION; NUCLEAR RECEPTOR SUBFAMILY 2, GROUP C, MEMBER 2; PROTEIN BINDING; REPETITIVE SEQUENCES, NUCLEIC ACID; SEQUENCE ANALYSIS, DNA; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS;

EID: 84872045276     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201207189     Document Type: Article

References (58)

1. Allshire, R.C., M. Dempster, and N.D. Hastie. 1989. Human telomeres contain at least three types of G-rich repeat distributed non-randomly. Nucleic Acids Res. 17:4611-4627. http://dx.doi.org/10.1093/nar/17.12.4611
2. Anderson, M.J., G. Casey, C.L. Fasching, and E.J. Stanbridge. 1994. Evidence that wild-type TP53, and not genes on either chromosome 1 or 11, controls the tumorigenic phenotype of the human fibrosarcoma HT1080. Genes Chromosomes Cancer. 9:266-281. http://dx.doi.org/10.1002/gcc .2870090407
3. Baird, D.M., A.J. Jeffreys, and N.J. Royle. 1995. Mechanisms underlying telomere repeat turnover, revealed by hypervariable variant repeat distribution patterns in the human Xp/Yp telomere. EMBO J. 14:5433-5443.
4. Baird, D.M., J. Coleman, Z.H. Rosser, and N.J. Royle. 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. http://dx.doi.org/10.1086/302721
5. Bechard, L.H., B.D. Butuner, G.J. Peterson, W. McRae, Z. Topcu, and M.J. McEachern. 2009. Mutant telomeric repeats in yeast can disrupt the negative regulation of recombination-mediated telomere maintenance and create an alternative lengthening of telomeres-like phenotype. Mol. Cell. Biol. 29:626-639. http://dx.doi.org/10.1128/MCB.00423-08
6. Bechter, O.E., Y. Zou, W. Walker, W.E. Wright, and J.W. Shay. 2004. Telomeric recombination in mismatch repair deficient human colon cancer cells after telomerase inhibition. Cancer Res. 64:3444-3451. http://dx.doi.org/10.1158/0008-5472.CAN-04-0323
7. Brault, M.E., and C. Autexier. 2011. Telomeric recombination induced by dysfunctional telomeres. Mol. Biol. Cell. 22:179-188. http://dx.doi.org/10.1091/mbc.E10-02-0173
8. Bryan, T.M., A. Englezou, J. Gupta, S. Bacchetti, and R.R. Reddel. 1995. Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J. 14:4240-4248.
9. Bryan, T.M., A. Englezou, L. Dalla-Pozza, M.A. Dunham, and R.R. Reddel. 1997. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med. 3:1271- 1274. http://dx.doi.org/10.1038/nm1197-1271
10. Celli, G.B., E.L. Denchi, and T. de Lange. 2006. Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination. Nat. Cell Biol. 8:885-890. http://dx.doi.org/10.1038/ ncb1444
11. Cesare, A.J., and J.D. Griffith. 2004. Telomeric DNA in ALT cells is characterized by free telomeric circles and heterogeneous t-loops. Mol. Cell. Biol. 24:9948-9957. http://dx.doi.org/10.1128/MCB.24.22.9948-9957.2004
12. Cesare, A.J., and R.R. Reddel. 2008. Telomere uncapping and alternative lengthening of telomeres. Mech. Ageing Dev. 129:99-108. http://dx.doi.org/ 10.1016/j.mad.2007.11.006
13. Cesare, A.J., Z. Kaul, S.B. Cohen, C.E. Napier, H.A. Pickett, A.A. Neumann, and R.R. Reddel. 2009. Spontaneous occurrence of telomeric DNA damage response in the absence of chromosome fusions. Nat. Struct. Mol. Biol. 16:1244-1251. http://dx.doi.org/10.1038/nsmb.1725
14. Coleman, J., D.M. Baird, and N.J. Royle. 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. http://dx.doi.org/10.1093/hmg/8.9.1637
15. Cui, S., K.E. Kolodziej, N. Obara, A. Amaral-Psarris, J. Demmers, L. Shi, J.D. Engel, F. Grosveld, J. Strouboulis, and O. Tanabe. 2011. Nuclear receptors TR2 and TR4 recruit multiple epigenetic transcriptional corepressors that associate specifically with the embryonic ?-type globin promoters in differentiated adult erythroid cells. Mol. Cell. Biol. 31:3298-3311. http:// dx.doi.org/10.1128/MCB.05310-11
16. d'Adda di Fagagna, F., P.M. Reaper, L. Clay-Farrace, H. Fiegler, P. Carr, T. Von Zglinicki, G. Saretzki, N.P. Carter, and S.P. Jackson. 2003. A DNA damage checkpoint response in telomere-initiated senescence. Nature. 426:194-198. http://dx.doi.org/10.1038/nature02118
17. Déjardin, J. 2012. How chromatin prevents genomic rearrangements: locus colocalization induced by transcription factor binding. Bioessays. 34:90-93. http://dx.doi.org/10.1002/bies.201100122
18. Déjardin, J., and R.E. Kingston. 2009. Purification of proteins associated with specific genomic Loci. Cell. 136:175-186. http://dx.doi.org/10.1016/ j.cell.2008.11.045
19. Dunham, M.A., A.A. Neumann, C.L. Fasching, and R.R. Reddel. 2000. Telomere maintenance by recombination in human cells. Nat. Genet. 26:447-450. http://dx.doi.org/10.1038/82586
20. Fasching, C.L., K. Bower, and R.R. Reddel. 2005. Telomerase-independent telomere length maintenance in the absence of alternative lengthening of telomeres-associated promyelocytic leukemia bodies. Cancer Res. 65:2722-2729. http://dx.doi.org/10.1158/0008-5472.CAN-04-2881
21. Griffith, J.D., L. Comeau, S. Rosenfield, R.M. Stansel, A. Bianchi, H. Moss, and T. de Lange. 1999. Mammalian telomeres end in a large duplex loop. Cell. 97:503-514. http://dx.doi.org/10.1016/S0092-8674(00)80760-6
22. Guiducci, C., M.A. Cerone, and S. Bacchetti. 2001. Expression of mutant telomerase in immortal telomerase-negative human cells results in cell cycle deregulation, nuclear and chromosomal abnormalities and rapid loss of viability. Oncogene. 20:714-725. http://dx.doi.org/10.1038/sj.onc.1204145
23. Hanaoka, S., A. Nagadoi, and Y. Nishimura. 2005. Comparison between TRF2 and TRF1 of their telomeric DNA-bound structures and DNA-binding activities. Protein Sci. 14:119-130. http://dx.doi.org/10.1110/ps.04983705
24. Harley, C.B., A.B. Futcher, and C.W. Greider. 1990. Telomeres shorten during ageing of human fibroblasts. Nature. 345:458-460. http://dx.doi.org/ 10.1038/345458a0
25. Heaphy, C.M., R.F. de Wilde, Y. Jiao, A.P. Klein, B.H. Edil, C. Shi, C. Bettegowda, F.J. Rodriguez, C.G. Eberhart, S. Hebbar, et al. 2011. Altered telomeres in tumors with ATRX and DAXX mutations. Science. 333:425. http://dx.doi.org/10.1126/science.1207313
26. Henson, J.D., and R.R. Reddel. 2010. Assaying and investigating Alternative Lengthening of Telomeres activity in human cells and cancers. FEBS Lett. 584:3800-3811. http://dx.doi.org/10.1016/j.febslet.2010.06.009
27. Henson, J.D., Y. Cao, L.I. Huschtscha, A.C. Chang, A.Y. Au, H.A. Pickett, and R.R. Reddel. 2009. DNA C-circles are specific and quantifiable markers of alternative-lengthening-of-telomeres activity. Nat. Biotechnol. 27:1181-1185. http://dx.doi.org/10.1038/nbt.1587
28. Hockemeyer, D., A.J. Sfeir, J.W. Shay, W.E. Wright, and T. de Lange. 2005. POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end. EMBO J. 24:2667-2678. http:// dx.doi.org/10.1038/sj.emboj.7600733
29. Jiang, W.Q., Z.H. Zhong, J.D. Henson, A.A. Neumann, A.C. Chang, and R.R. Reddel. 2005. Suppression of alternative lengthening of telomeres by Sp100-mediated sequestration of the MRE11/RAD50/NBS1 complex. Mol. Cell. Biol. 25:2708-2721. http://dx.doi.org/10.1128/MCB.25.7 .2708-2721.2005
30. Kato, S., H. Sasaki, M. Suzawa, S. Masushige, L. Tora, P. Chambon, and H. Gronemeyer. 1995. Widely spaced, directly repeated PuGGTCA elements act as promiscuous enhancers for different classes of nuclear receptors. Mol. Cell. Biol. 15:5858-5867.
31. Kim, M.M., M.A. Rivera, I.L. Botchkina, R. Shalaby, A.D. Thor, and E.H. Blackburn. 2001. A low threshold level of expression of mutant-template telomerase RNA inhibits human tumor cell proliferation. Proc. Natl. Acad. Sci. USA. 98:7982-7987. http://dx.doi.org/10.1073/pnas.131211098
32. Li, H., and R. Durbin. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 25:1754-1760. http://dx.doi .org/10.1093/bioinformatics/btp324
33. Li, S., J.E. Rosenberg, A.A. Donjacour, I.L. Botchkina, Y.K. Hom, G.R. Cunha, and E.H. Blackburn. 2004. Rapid inhibition of cancer cell growth induced by lentiviral delivery and expression of mutant-template telomerase RNA and anti-telomerase short-interfering RNA. Cancer Res. 64:4833-4840. http://dx.doi.org/10.1158/0008-5472.CAN-04-0953
34. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, and R. Durbin; 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics. 25:2078-2079. http://dx.doi.org/10.1093/bioinformatics/btp352
35. Londoño-Vallejo, J.A., H. Der-Sarkissian, L. Cazes, S. Bacchetti, and R.R. Reddel. 2004. Alternative lengthening of telomeres is characterized by high rates of telomeric exchange. Cancer Res. 64:2324-2327. http://dx.doi.org/10.1158/0008-5472.CAN-03-4035
36. Lovejoy, C.A., W. Li, S. Reisenweber, S. Thongthip, J. Bruno, T. de Lange, S. De, J.H. Petrini, P.A. Sung, M. Jasin, et al; ALT Starr Cancer Consortium. 2012. Loss of ATRX, genome instability, and an altered DNA damage response are hallmarks of the alternative lengthening of telomeres pathway. PLoS Genet. 8:e1002772. http://dx.doi.org/10.1371/journal.pgen.1002772
37. Marusíc, L., M. Anton, A. Tidy, P. Wang, B. Villeponteau, and S. Bacchetti. 1997. Reprogramming of telomerase by expression of mutant telomerase RNA template in human cells leads to altered telomeres that correlate with reduced cell viability. Mol. Cell. Biol. 17:6394-6401.
38. Moyzis, R.K., J.M. Buckingham, L.S. Cram, M. Dani, L.L. Deaven, M.D. Jones, J. Meyne, R.L. Ratliff, and J.R. Wu. 1988. A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc. Natl. Acad. Sci. USA. 85:6622-6626. http://dx.doi .org/10.1073/pnas.85.18.6622
39. Muntoni, A., A.A. Neumann, M. Hills, and R.R. Reddel. 2009. Telomere elongation involves intra-molecular DNA replication in cells utilizing alternative lengthening of telomeres. Hum. Mol. Genet. 18:1017-1027. http://dx.doi.org/10.1093/hmg/ddn436
40. Nabetani, A., and F. Ishikawa. 2009. Unusual telomeric DNAs in human telomerase- negative immortalized cells. Mol. Cell. Biol. 29:703-713. http:// dx.doi.org/10.1128/MCB.00603-08
41. Palm, W., and T. de Lange. 2008. How shelterin protects mammalian telomeres. Annu. Rev. Genet. 42:301-334. http://dx.doi.org/10.1146/annurev.genet .41.110306.130350
42. Perrem, K., T.M. Bryan, A. Englezou, T. Hackl, E.L. Moy, and R.R. Reddel. 1999. Repression of an alternative mechanism for lengthening of telomeres in somatic cell hybrids. Oncogene. 18:3383-3390. http://dx.doi .org/10.1038/sj.onc.1202752
43. Perrem, K., L.M. Colgin, A.A. Neumann, T.R. Yeager, and R.R. Reddel. 2001. Coexistence of alternative lengthening of telomeres and telomerase in hTERT-transfected GM847 cells. Mol. Cell. Biol. 21:3862-3875. http:// dx.doi.org/10.1128/MCB.21.12.3862-3875.2001
44. Pickett, H.A., A.J. Cesare, R.L. Johnston, A.A. Neumann, and R.R. Reddel. 2009. Control of telomere length by a trimming mechanism that involves generation of t-circles. EMBO J. 28:799-809. http://dx.doi.org/10.1038/ emboj.2009.42
45. Sandelin, A., and W.W. Wasserman. 2005. Prediction of nuclear hormone receptor response elements. Mol. Endocrinol. 19:595-606. http://dx.doi.org/10.1210/me.2004-0101 Schwartzentruber, J., A. Korshunov, X.Y. Liu, D.T. Jones, E. Pfaff, K.
46. Jacob, D. Sturm, A.M. Fontebasso, D.A. Quang, M. Tönjes, et al. 2012. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature. 482:226-231. http://dx.doi.org/10.1038/nature10833
47. Sfeir, A., S. Kabir, M. van Overbeek, G.B. Celli, and T. de Lange. 2010. Loss of Rap1 induces telomere recombination in the absence of NHEJ or a DNA damage signal. Science. 327:1657-1661. http://dx.doi.org/10.1126/science.1185100
48. Shay, J.W., and S. Bacchetti. 1997. A survey of telomerase activity in human cancer. Eur. J. Cancer. 33:787-791. http://dx.doi.org/10.1016/S0959- 8049(97)00062-2
49. Stern, J.L., K.G. Zyner, H.A. Pickett, S.B. Cohen, and T.M. Bryan. 2012. Telomerase recruitment requires both TCAB1 and Cajal bodies independently. Mol. Cell. Biol. 32:2384-2395. http://dx.doi.org/10.1128/MCB.00379-12
50. Stohr, B.A., and E.H. Blackburn. 2008. ATM mediates cytotoxicity of a mutant telomerase RNA in human cancer cells. Cancer Res. 68:5309-5317. http://dx.doi.org/10.1158/0008-5472.CAN-08-0504 Sullivan, B.A. 2010. Optical mapping of protein-DNA complexes on chromatin fibers. Methods Mol. Biol. 659:99-115. http://dx.doi.org/10.1007/ 978-1-60761-789-1_7
51. Sullivan, B.A. 2010. Optical mapping of protein-DNA complexes on chromatin fibers. Methods Mol. Biol. 659:99-115. http://dx.doi.org/10.1007/ 978-1-60761-789-1_7
52. Tokutake, Y., T. Matsumoto, T. Watanabe, S. Maeda, H. Tahara, S. Sakamoto, H. Niida, M. Sugimoto, T. Ide, and Y. Furuichi. 1998. Extra-chromosomal telomere repeat DNA in telomerase-negative immortalized cell lines. Biochem. Biophys. Res. Commun. 247:765-772. http://dx.doi.org/10.1006/bbrc.1998.8876
53. van Steensel, B., A. Smogorzewska, and T. de Lange. 1998. TRF2 protects human telomeres from end-to-end fusions. Cell. 92:401-413. http://dx.doi.org/10.1016/S0092-8674(00)80932-0
54. Varley, H., H.A. Pickett, J.L. Foxon, R.R. Reddel, and N.J. Royle. 2002. Molecular characterization of inter-telomere and intra-telomere mutations in human ALT cells. Nat. Genet. 30:301-305. http://dx.doi.org/10.1038/ng834
55. Wang, R.C., A. Smogorzewska, and T. de Lange. 2004. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell. 119: 355-368. http://dx.doi.org/10.1016/j.cell.2004.10.011
56. Wong, J.M., and K. Collins. 2006. Telomerase RNA level limits telomere maintenance in X-linked dyskeratosis congenita. Genes Dev. 20:2848-2858. http://dx.doi.org/10.1101/gad.1476206
57. Yeager, T.R., A.A. Neumann, A. Englezou, L.I. Huschtscha, J.R. Noble, and R.R. Reddel. 1999. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59:4175-4179.
58. Zhong, Z.H., W.Q. Jiang, A.J. Cesare, A.A. Neumann, R. Wadhwa, and R.R. Reddel. 2007. Disruption of telomere maintenance by depletion of the MRE11/RAD50/NBS1 complex in cells that use alternative lengthening of telomeres. J. Biol. Chem. 282:29314-29322. http://dx.doi.org/10.1074/ jbc.M701413200