Lack of TRF2 in ALT cells causes PML-dependent p53 activation and loss of telomeric DNA

Journal of Cell Biology

Volumn 179, Issue 5, 2007, Pages 855-867

  D'Alcontres, Martina Stagno ^a   Mendez Bermudez, Aaron ^a   Foxon, Jennifer L ^a   Royle, Nicola J ^a   Salomoni, Paolo ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN P21; PROTEIN P53; TELOMERIC REPEAT BINDING FACTOR 2;

ARTICLE; CELL AGING; CELL DEATH; CELL NUCLEUS; CELL PROTECTION; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; TELOMERE; TUMOR CELL;

CELL AGING; CELL CYCLE; CELL LINE, TUMOR; DNA, NEOPLASM; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; INTRANUCLEAR INCLUSION BODIES; NEOPLASM PROTEINS; NUCLEAR PROTEINS; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 2; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 36849003494     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200703020     Document Type: Article

References (40)

1. Bartkova, J., N. Rezaei, M. Liontos, P. Karakaidos, D. Kletsas, N. Issaeva, L.V. Vassiliou, E. Kolettas, K. Niforou, V.C. Zoumpourlis, et al. 2006. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature. 444:633-637.
2. Bernardi, R., P.P. Scaglioni, S. Bergmann, H.F. Horn, K.H. Vousden, and P.P. Pandolfi. 2004. PML regulates p53 stability by sequestering Mdm2 to the nucleolus. Nat. Cell Biol. 6:665-672.
3. Bi, X., D. Srikanta, L. Fanti, S. Pimpinelli, R. Badugu, R. Kellum, and Y.S. Rong. 2005. Drosophila ATM and ATR checkpoint kinases control partially redundant pathways for telomere maintenance. Proc. Natl. Acad. Sci. USA. 102:15167-15172.
4. Blanco, R., P. Munoz, J.M. Flores, P. Klatt, and M.A. Blasco. 2007. Telomerase abrogation dramatically accelerates TRF2-induced epithelial carcinogenesis. Genes Dev. 21:206-220.
5. Brinkley, B.R. 2001. Managing the centrosome numbers game: from chaos to stability in cancer cell division. Trends Cell Biol. 11:18-21.
6. 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.
7. de Lange, T. 2002. Protection of mammalian telomeres. Oncogene. 21:532-540.
8. de Lange, T. 2005. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19:2100-2110.
9. de Stanchina, E., E. Querido, M. Narita, R.V. Davuluri, P.P. Pandolfi, G. Ferbeyre, and S.W. Lowe. 2004. PML is a direct p53 target that modulates p53 effector functions. Mol. Cell. 13:523-535.
10. Di Micco, R., M. Fumagalli, A. Cicalese, S. Piccinin, P. Gasparini, C. Luise, C. Schurra, M. Garre, P.G. Nuciforo, A. Bensimon, et al. 2006. Oncogene-induced senescence is a DNA damage response triggered by DNA hyperreplication. Nature. 444:638-642.
11. Jeffreys, A.J., N.J. Royle, V. Wilson, and Z. Wong. 1988. Spontaneous mutation rates to new length alleles at tandem-repetitive hypervariable loci in human DNA. Nature. 332:278-281.
12. Jiang, W.Q., Z.H. Zhong, J.D. Henson, and R.R. Reddel. 2007. Identification of candidate alternative lengthening of telomeres genes by methionine restriction and RNA interference. Oncogene. 26:4635-4647.
13. Karlseder, J., D. Broccoli, Y. Dai, S. Hardy, and T. de Lange. 1999. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science. 283:1321-1325.
14. Karlseder, J., A. Smogorzewska, and T. de Lange. 2002. Senescence induced by altered telomere state, not telomere loss. Science. 295:2446-2449.
15. Karlseder, J., K. Hoke, O.K. Mirzoeva, C. Bakkenist, M.B. Kastan, J.H. Petrini, and T. Lange Td. 2004. The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLoS Biol. 2:E240.
16. Kirsch-Volders, M., A. Vanhauwaert, M. De Boeck, and I. Decordier. 2002. Importance of detecting numerical versus structural chromosome aberrations. Mutat. Res. 504:137-148.
17. Lansdorp, P.M., N.P. Verwoerd, F.M. van de Rijke, V. Dragowska, M.T. Little, R.W. Dirks, A.K. Raap, and H.J. Tanke. 1996. Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet. 5:685-691.
18. Londono-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.
19. Mallette, F.A., M.F. Gaumont-Leclerc, and G. Ferbeyre. 2007. The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence. Genes Dev. 21:43-48.
20. Mihara, K., M. Iijima, T. Kondo, and M. Namba. 1996. Selective expression of mutated p53 in human cells immortalized with either 4-nitroquinoline 1-oxide or 60Co gamma rays. Cell Struct. Funct. 21:111-116.
21. Munoz, P., R. Blanco, J.M. Flores, and M.A. Blasco. 2005. XPF nuclease-dependent telomere loss and increased DNA damage in mice overexpressing TRF2 result in premature aging and cancer. Nat. Genet. 37:1063-1071.
22. Muntoni, A., and R.R. Reddel. 2005. The first molecular details of ALT in human tumor cells. Hum. Mol. Genet. 14:R191-R196.
23. Naka, K., K. Ikeda, and N. Motoyama. 2002. Recruitment of NBS1 into PML oncogenic domains via interaction with SP100 protein. Biochem. Biophys. Res. Commun. 299:863-871.
24. Oh, B.K., Y.J. Kim, C. Park, and Y.N. Park. 2005. Up-regulation of telomere-binding proteins, TRF1, TRF2, and TIN2 is related to telomere shortening during human multistep hepatocarcinogenesis. Am. J. Pathol. 166:73-80.
25. Pearson, M., R. Carbone, C. Sebastiani, M. Cioce, M. Fagioli, S. Saito, Y. Higashimoto, E. Appella, S. Minucci, P.P. Pandolfi, and P.G. Pelicci. 2000. PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature. 406:207-210.
26. Potts, P.R., and H. Yu. 2007. The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat. Struct. Mol. Biol. 14:581-590.
27. Razak, Z.R., R.J. Varkonyi, M. Kulp-McEliece, C. Caslini, J.R. Testa, M.E. Murphy, and D. Broccoli. 2004. p53 differentially inhibits cell growth depending on the mechanism of telomere maintenance. Mol. Cell. Biol. 24:5967-5977.
28. Rufer, N., W. Dragowska, G. Thornbury, E. Roosnek, and P.M. Lansdorp. 1998. Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry. Nat. Biotechnol. 16:743-747.
29. Salomoni, P., and P.P. Pandolfi. 2002. The role of PML in tumor suppression. Cell. 108:165-170.
30. Takai, H., A. Smogorzewska, and T. de Lange. 2003. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13:1549-1556.
31. van Steensel, B., A. Smogorzewska, and T. de Lange. 1998. TRF2 protects human telomeres from end-to-end fusions. Cell. 92:401-413.
32. Verdun, R.E., and J. Karlseder. 2006. The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell. 127:709-720.
33. Verdun, R.E., L. Crabbe, C. Haggblom, and J. Karlseder. 2005. Functional human telomeres are recognized as DNA damage in G2 of the cell cycle. Mol. Cell. 20:551-561.
34. Wang, R.C., A. Smogorzewska, and T. de Lange. 2004. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell. 119:355-368.
35. Wu, G., W.H. Lee, and P.L. Chen. 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.
36. Wu, G., X. Jiang, W.H. Lee, and P.L. Chen. 2003. Assembly of functional ALT-associated promyelocytic leukemia bodies requires Nijmegen Breakage Syndrome 1. Cancer Res. 63:2589-2595.
37. Xu, L., and E.H. Blackburn. 2004. Human Rif1 protein binds aberrant telomeres and aligns along anaphase midzone microtubules. J. Cell Biol. 167:819-830.
38. 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.
39. Zhu, X.D., B. Kuster, M. Mann, J.H. Petrini, and T. de Lange. 2000. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25:347-352.
40. Zijlmans, J.M., U.M. Martens, S.S. Poon, A.K. Raap, H.J. Tanke, R.K. Ward, and P.M. Lansdorp. 1997. Telomeres in the mouse have large interchromosomal variations in the number of T2AG3 repeats. Proc. Natl. Acad. Sci. USA. 94:7423-7428.