Molecular mechanisms of activity and derepression of alternative lengthening of telomeres

Nature Structural and Molecular Biology

Volumn 22, Issue 11, 2015, Pages 875-880

  Pickett, Hilda A ^a   Reddel, Roger R ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; DNA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HORMONE RECEPTOR; NUCLEOPROTEIN; PROTEIN; PROTEIN NURD; PROTEIN ZNF827; UNCLASSIFIED DRUG; DNA HELICASE; NUCLEAR PROTEIN;

ALTERNATIVE LENGTHENING OF TELOMERE; ARABIDOPSIS THALIANA; CAENORHABDITIS ELEGANS; CELL CYCLE PROGRESSION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DEACETYLATION; DNA DAMAGE; DNA SEQUENCE; DNA SYNTHESIS; EUKARYOTE; HISTONE ACETYLATION; HUMAN; IMMORTALIZED CELL LINE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RETROPOSON; REVERSE TRANSCRIPTION; REVIEW; STRESS; TELOMERE HOMEOSTASIS; HOMOLOGOUS RECOMBINATION; METABOLISM; TELOMERE;

DNA HELICASES; HOMOLOGOUS RECOMBINATION; NUCLEAR PROTEINS; TELOMERE; TELOMERE HOMEOSTASIS;

EID: 84947911388     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3106     Document Type: Review

References (81)

1. Bryan, T. M., Englezou, A., Dalla-Pozza, L., Dunham, M. A. & Reddel, R. R. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med. 3, 1271-1274 (1997).
2. Heaphy, C. M. et al. Prevalence of the alternative lengthening of telomeres telomere maintenance mechanism in human cancer subtypes. Am. J. Pathol. 179, 1608-1615 (2011).
3. Greider, C. W. & Blackburn, E. H. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337, 331-337 (1989).
4. Reddel, R. R., Bryan, T. M. & Murnane, J. P. Immortalized cells with no detectable telomerase activity: A review. Biochemistry (Mosc.) 62, 1254-1262 (1997).
5. Dunham, M. A., Neumann, A. A., Fasching, C. L. & Reddel, R. R. Telomere maintenance by recombination in human cells. Nat. Genet. 26, 447-450 (2000).
6. Neumann, A. A. et al. Alternative lengthening of telomeres in normal mammalian somatic cells. Genes Dev. 27, 18-23 (2013).
7. O'Sullivan, R. J. et al. Rapid induction of alternative lengthening of telomeres by depletion of the histone chaperone ASF1. Nat. Struct. Mol. Biol. 21, 167-174 (2014).
8. Muntoni, A., Neumann, A. A., Hills, M. & Reddel, R. R. Telomere elongation involves intra-molecular DNA replication in cells utilizing alternative lengthening of telomeres. Hum. Mol. Genet. 18, 1017-1027 (2009).
9. McEachern, M. J. & Haber, J. E. Break-induced replication and recombinational telomere elongation in yeast. Annu. Rev. Biochem. 75, 111-135 (2006).
10. Natarajan, S. & McEachern, M. J. Recombinational telomere elongation promoted by DNA circles. Mol. Cell. Biol. 22, 4512-4521 (2002).
11. Cesare, A. J. & Reddel, R. R. Alternative lengthening of telomeres: models, mechanisms and implications. Nat. Rev. Genet. 11, 319-330 (2010).
12. Wilson, J. S. et al. Localization-dependent and-independent roles of SLX4 in regulating telomeres. Cell Rep. 4, 853-860 (2013).
13. Wan, B. et al. SLX4 assembles a telomere maintenance toolkit by bridging multiple endonucleases with telomeres. Cell Rep. 4, 861-869 (2013).
14. Bhattacharyya, S. et al. Telomerase associated protein 1, HSP90 and topoisomerase IIa 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 (2009).
15. Conomos, D., Reddel, R. R. & Pickett, H. A. NuRD-ZNF827 recruitment to telomeres creates a molecular scaffold for homologous recombination. Nat. Struct. Mol. Biol. 21, 760-770 (2014).
16. Palm, W. & de Lange, T. How shelterin protects mammalian telomeres. Annu. Rev. Genet. 42, 301-334 (2008).
17. Sung, P. & Klein, H. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell Biol. 7, 739-750 (2006).
18. Flynn, R. L. et al. TERRA and hnRNPA1 orchestrate an RPA-to-POT1 switch on telomeric single-stranded DNA. Nature 471, 532-536 (2011).
19. Krejci, L., Altmannova, V., Spirek, M. & Zhao, X. Homologous recombination and its regulation. Nucleic Acids Res. 40, 5795-5818 (2012).
20. Maloisel, L., Fabre, F. & Gangloff, S. DNA polymerase is preferentially recruited during homologous recombination to promote heteroduplex DNA extension. Mol. Cell. Biol. 28, 1373-1382 (2008).
21. Sharma, S. et al. REV1 and polymerase facilitate homologous recombination repair. Nucleic Acids Res. 40, 682-691 (2012).
22. Jiang, W. Q. et al. Induction of alternative lengthening of telomeres-associated PML bodies by p53/p21 requires HP1 proteins. J. Cell Biol. 185, 797-810 (2009).
23. Lydeard, J. R., Jain, S., Yamaguchi, M. & Haber, J. E. Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448, 820-823 (2007).
24. Wyatt, H. D., Sarbajna, S., Matos, J. & West, S. C. Coordinated actions of SLX1-SLX4 and MUS81-EME1 for Holliday junction resolution in human cells. Mol. Cell 52, 234-247 (2013).
25. Sarbajna, S., Davies, D. & West, S. C. Roles of SLX1-SLX4, MUS81-EME1, and GEN1 in avoiding genome instability and mitotic catastrophe. Genes Dev. 28, 1124-1136 (2014).
26. Pepe, A. & West, S. C. MUS81-EME2 promotes replication fork restart. Cell Rep. 7, 1048-1055 (2014).
27. Opresko, P. L. et al. Telomere binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem. 277, 41110-41119 (2002).
28. Sarkar, J. et al. SLX4 contributes to telomere preservation and regulated processing of telomeric joint molecule intermediates. Nucleic Acids Res. 43, 5912-5923 (2015).
29. Dimitrova, N., Chen, Y. C., Spector, D. L. & de Lange, T. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456, 524-528 (2008).
30. Cesare, A. J. et al. Spontaneous occurrence of telomeric DNA damage response in the absence of chromosome fusions. Nat. Struct. Mol. Biol. 16, 1244-1251 (2009).
31. Molenaar, C. et al. Visualizing telomere dynamics in living mammalian cells using PNA probes. EMBO J. 22, 6631-6641 (2003).
32. Yeager, T. R. et al. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59, 4175-4179 (1999).
33. Draskovic, I. et al. Probing PML body function in ALT cells reveals spatiotemporal requirements for telomere recombination. Proc. Natl. Acad. Sci. USA 106, 15726-15731 (2009).
34. Fasching, C. L., Neumann, A. A., Muntoni, A., Yeager, T. R. & Reddel, R. R. DNA damage induces alternative lengthening of telomeres (ALT) associated promyelocytic leukemia bodies that preferentially associate with linear telomeric DNA. Cancer Res. 67, 7072-7077 (2007).
35. Cho, N. W., Dilley, R. L., Lampson, M. A. & Greenberg, R. A. Interchromosomal homology searches drive directional ALT telomere movement and synapsis. Cell 159, 108-121 (2014).
36. Zhao, W. & Sung, P. Significance of ligand interactions involving Hop2-Mnd1 and the RAD51 and DMC1 recombinases in homologous DNA repair and XX ovarian dysgenesis. Nucleic Acids Res. 43, 4055-4066 (2015).
37. Tommerup, H., Dousmanis, A. & de Lange, T. Unusual chromatin in human telomeres. Mol. Cell. Biol. 14, 5777-5785 (1994).
38. Galati, A. et al. TRF1 and TRF2 binding to telomeres is modulated by nucleosomal organization. Nucleic Acids Res. 43, 5824-5837 (2015).
39. Episkopou, H. et al. Alternative lengthening of telomeres is characterized by reduced compaction of telomeric chromatin. Nucleic Acids Res. 42, 4391-4405 (2014).
40. Déjardin, J. & Kingston, R. E. Purification of proteins associated with specific genomic loci. Cell 136, 175-186 (2009).
41. Michishita, E. et al. SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 452, 492-496 (2008).
42. Blasco, M. A. The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet. 8, 299-309 (2007).
43. García-Cao, M., O'Sullivan, R., Peters, A. H., Jenuwein, T. & Blasco, M. A. Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat. Genet. 36, 94-99 (2004).
44. Heaphy, C. M. et al. Altered telomeres in tumors with ATRX and DAXX mutations. Science 333, 425 (2011).
45. Lovejoy, C. A. et al. Loss of ATRX, genome instability, and an altered DNA damage response are hallmarks of the alternative lengthening of telomeres pathway. PLoS Genet. 8, e1002772 (2012).
46. Bower, K. et al. Loss of wild-type ATRX expression in somatic cell hybrids segregates with activation of alternative lengthening of telomeres. PLoS ONE 7, e50062 (2012).
47. Schwartzentruber, J. et al. Driver mutations in histone H3. 3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482, 226-231 (2012).
48. Lee, J. C. et al. Alternative lengthening of telomeres and loss of ATRX are frequent events in pleomorphic and dedifferentiated liposarcomas. Mod. Pathol. 28, 1064-1073 (2015).
49. Napier, C. E. et al. ATRX represses alternative lengthening of telomeres. Oncotarget 6, 16543-16558 (2015).
50. Wong, L. H. et al. ATRX interacts with H3. 3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res. 20, 351-360 (2010).
51. Law, M. J. et al. ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner. Cell 143, 367-378 (2010).
52. Clynes, D. et al. Suppression of the alternative lengthening of telomere pathway by the chromatin remodelling factor ATRX. Nat. Commun. 6, 7538 (2015).
53. Ritchie, K. et al. Loss of ATRX leads to chromosome cohesion and congression defects. J. Cell Biol. 180, 315-324 (2008).
54. Conomos, D. et al. Variant repeats are interspersed throughout the telomeres and recruit nuclear receptors in ALT cells. J. Cell Biol. 199, 893-906 (2012).
55. Lee, M. et al. Telomere extension by telomerase and ALT generates variant repeats by mechanistically distinct processes. Nucleic Acids Res. 42, 1733-1746 (2014).
56. Baird, D. M., Jeffreys, A. J. & Royle, N. J. Mechanisms underlying telomere repeat turnover, revealed by hypervariable variant repeat distribution patterns in the human Xp/Yp telomere. EMBO J. 14, 5433-5443 (1995).
57. Baird, D. M., Coleman, J., Rosser, Z. H. & Royle, N. J. 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 (2000).
58. Varley, H., Pickett, H. A., Foxon, J. L., Reddel, R. R. & Royle, N. J. Molecular characterization of inter-telomere and intra-telomere mutations in human ALT cells. Nat. Genet. 30, 301-305 (2002).
59. Marzec, P. et al. Nuclear-receptor-mediated telomere insertion leads to genome instabiltiy in ALT cancers. Cell 160, 913-927 (2015).
60. Kilburn, A. E., Shea, M. J., Sargent, R. G. & Wilson, J. H. Insertion of a telomere repeat sequence into a mammalian gene causes chromosome instability. Mol. Cell. Biol. 21, 126-135 (2001).
61. Sakellariou, D., Chiourea, M., Raftopoulou, C. & Gagos, S. Alternative lengthening of telomeres: recurrent cytogenetic aberrations and chromosome stability under extreme telomere dysfunction. Neoplasia 15, 1301-1313 (2013).
62. Sfeir, A. et al. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138, 90-103 (2009).
63. Croteau, D. L., Popuri, V., Opresko, P. L. & Bohr, V. A. Human RecQ helicases in DNA repair, recombination, and replication. Annu. Rev. Biochem. 83, 519-552 (2014).
64. Sarek, G., Vannier, J. B., Panier, S., Petrini, J. H. & Boulton, S. J. TRF2 recruits RTEL1 to telomeres in S phase to promote T-loop unwinding. Mol. Cell 57, 622-635 (2015).
65. León-Ortiz, A. M., Svendsen, J. & Boulton, S. J. Metabolism of DNA secondary structures at the eukaryotic replication fork. DNA Repair (Amst.) 19, 152-162 (2014).
66. Denchi, E. L. & de Lange, T. Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 448, 1068-1071 (2007).
67. Flynn, R. L. et al. Alternative lengthening of telomeres renders cancer cells hypersensitive to ATR inhibitors. Science 347, 273-277 (2015).
68. Nakamura, T. M. & Cech, T. R. Reversing time: origin of telomerase. Cell 92, 587-590 (1998).
69. Eickbush, T. H. Telomerase and retrotransposons: which came first? Science 277, 911-912 (1997).
70. de Lange, T. T-loops and the origin of telomeres. Nat. Rev. Mol. Cell Biol. 5, 323-329 (2004).
71. Muntoni, A. & Reddel, R. R. The first molecular details of ALT in human tumor cells. Hum. Mol. Genet. 14, Spec No. 2, R191-R196 (2005).
72. Biessmann, H. & Mason, J. M. Telomere maintenance without telomerase. Chromosoma 106, 63-69 (1997).
73. Lundblad, V. & Blackburn, E. H. An alternative pathway for yeast telomere maintenance rescues est1? senescence. Cell 73, 347-360 (1993).
74. McEachern, M. J. & Blackburn, E. H. Cap-prevented recombination between terminal telomeric repeat arrays (telomere CPR) maintains telomeres in Kluyveromyces lactis lacking telomerase. Genes Dev. 10, 1822-1834 (1996).
75. Lackner, D. H., Raices, M., Maruyama, H., Haggblom, C. & Karlseder, J. Organismal propagation in the absence of a functional telomerase pathway in Caenorhabditis elegans. EMBO J. 31, 2024-2033 (2012).
76. Cheng, C., Shtessel, L., Brady, M. M. & Ahmed, S. Caenorhabditis elegans POT-2 telomere protein represses a mode of alternative lengthening of telomeres with normal telomere lengths. Proc. Natl. Acad. Sci. USA 109, 7805-7810 (2012).
77. Riha, K., McKnight, T. D., Griffing, L. R. & Shippen, D. E. Living with genome instability: plant responses to telomere dysfunction. Science 291, 1797-1800 (2001).
78. Niida, H. et al. Telomere maintenance in telomerase-deficient mouse embryonic stem cells: characterization of an amplified telomeric DNA. Mol. Cell. Biol. 20, 4115-4127 (2000).
79. Bryan, T. M., Englezou, A., Gupta, J., Bacchetti, S. & Reddel, R. R. Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J. 14, 4240-4248 (1995).
80. Rogan, E. M. et al. Alterations in p53 and p16INK4 expression and telomere length during spontaneous immortalization of Li-Fraumeni syndrome fibroblasts. Mol. Cell. Biol. 15, 4745-4753 (1995).
81. Herrera, E., Martinez, C. & Blasco, M. A. Impaired germinal center reaction in mice with short telomeres. EMBO J. 19, 472-481 (2000).