Alternative lengthening of telomeres (ALT) and chromatin: Is there a connection?

Biochimie

Volumn 90, Issue 1, 2008, Pages 5-12

  Nittis, Thalia ^a   Guittat, Lionel ^a   Stewart, Sheila A ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

Alternative lengthening of telomeres; DNA methylation; Epigenetic modifications; Histone methylation; Telomere

Indexed keywords

ANTINEOPLASTIC AGENT; HISTONE;

ANTINEOPLASTIC ACTIVITY; CARCINOGENESIS; CELL TYPE; CHROMATIN; CHROMATIN STRUCTURE; CHROMOSOME SIZE; DNA METHYLATION; ENZYME ACTIVATION; EPIGENETICS; HUMAN; MEDICAL LITERATURE; MESENCHYME CELL; NONHUMAN; PREVALENCE; PROTEIN METHYLATION; PROTEIN STRUCTURE; REVIEW; TELOMERE; TUMOR;

ANIMALS; CHROMATIN; EPIGENESIS, GENETIC; HISTONES; HUMANS; METHYLATION; NEOPLASMS; RECOMBINATION, GENETIC; SISTER CHROMATID EXCHANGE; TELOMERASE; TELOMERE;

EID: 36749043110     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2007.08.009     Document Type: Review

References (69)

1. Griffith J.D., Comeau L., Rosenfield S., Stansel R.M., Bianchi A., Moss H., and de Lange T. Mammalian telomeres end in a large duplex loop. Cell 97 (1999) 503-514
2. Blackburn E.H. Structure and function of telomeres. Nature 350 (1991) 569-573
3. Blackburn E.H. Switching and signaling at the telomere. Cell 106 (2001) 661-673
4. Harley C.B., Futcher A.B., and Greider C.W. Telomeres shorten during ageing of human fibroblasts. Nature 345 (1990) 458-460
5. Wei W., and Sedivy J.M. Differentiation between senescence (M1) and crisis (M2) in human fibroblast cultures. Exp. Cell Res. 253 (1999) 519-522
6. Shay J.W., and Roninson I.B. Hallmarks of senescence in carcinogenesis and cancer therapy. Oncogene 23 (2004) 2919-2933
7. Kim N.W., Piatyszek M.A., Prowse K.R., Harley C.B., West M.D., Ho P.L., Coviello G.M., Wright W.E., Weinrich S.L., and Shay J.W. Specific association of human telomerase activity with immortal cells and cancer. Science 266 (1994) 2011-2015
8. Hahn W.C., Stewart S.A., Brooks M.W., York S.G., Eaton E., Kurachi A., Beijersbergen R.L., Knoll J.H., Meyerson M., and Weinberg R.A. Inhibition of telomerase limits the growth of human cancer cells. Nat. Med. 5 (1999) 1164-1170
9. Dunham M.A., Neumann A.A., Fasching C.L., and Reddel R.R. Telomere maintenance by recombination in human cells. Nat. Genet. 26 (2000) 447-450
10. Yeager T.R., Neumann A.A., Englezou A., Huschtscha L.I., Noble J.R., and Reddel R.R. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59 (1999) 4175-4179
11. Henson J.D., Hannay J.A., McCarthy S.W., Royds J.A., Yeager T.R., Robinson R.A., Wharton S.B., Jellinek D.A., Arbuckle S.M., Yoo J., Robinson B.G., Learoyd D.L., Stalley P.D., Bonar S.F., Yu D., Pollock R.E., and Reddel R.R. A robust assay for alternative lengthening of telomeres in tumors shows the significance of alternative lengthening of telomeres in sarcomas and astrocytomas. Clin. Cancer Res. 11 (2005) 217-225
12. Costa A., Daidone M.G., Daprai L., Villa R., Cantu S., Pilotti S., Mariani L., Gronchi A., Henson J.D., Reddel R.R., and Zaffaroni N. Telomere maintenance mechanisms in liposarcomas: association with histologic subtypes and disease progression. Cancer Res. 66 (2006) 8918-8924
13. Muntoni A., and Reddel R.R. The first molecular details of ALT in human tumor cells. Hum. Mol. Genet. 14 Spec No. 2 (2005) R191-R196
14. Bechter O.E., Zou Y., Walker W., Wright W.E., and Shay J.W. Telomeric recombination in mismatch repair deficient human colon cancer cells after telomerase inhibition. Cancer Res. 64 (2004) 3444-3451
15. Lundblad V., and Blackburn E.H. An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell 73 (1993) 347-360
16. Teng S.C., and Zakian V.A. Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol. Cell Biol. 19 (1999) 8083-8093
17. Chen Q., Ijpma A., and Greider C.W. Two survivor pathways that allow growth in the absence of telomerase are generated by distinct telomere recombination events. Mol. Cell Biol. 21 (2001) 1819-1827
18. Kass-Eisler A., and Greider C.W. Recombination in telomere-length maintenance. Trends Biochem. Sci. 25 (2000) 200-204
19. Reddel R.R., Bryan T.M., Colgin L.M., Perrem K.T., and Yeager T.R. Alternative lengthening of telomeres in human cells. Radiat. Res. 155 (2001) 194-200
20. Bechter O.E., Zou Y., Shay J.W., and Wright W.E. Homologous recombination in human telomerase-positive and ALT cells occurs with the same frequency. EMBO Rep. 4 (2003) 1138-1143
21. Jeyapalan J.N., Varley H., Foxon J.L., Pollock R.E., Jeffreys A.J., Henson J.D., Reddel R.R., and Royle N.J. Activation of the ALT pathway for telomere maintenance can affect other sequences in the human genome. Hum. Mol. Genet. 14 (2005) 1785-1794
22. Londono-Vallejo J.A., Der-Sarkissian H., Cazes L., Bacchetti S., and Reddel R.R. Alternative lengthening of telomeres is characterized by high rates of telomeric exchange. Cancer Res. 64 (2004) 2324-2327
23. Bailey S.M., Brenneman M.A., and Goodwin E.H. Frequent recombination in telomeric DNA may extend the proliferative life of telomerase-negative cells. Nucleic Acids Res. 32 (2004) 3743-3751
24. Stavropoulos D.J., Bradshaw P.S., Li X., Pasic I., Truong K., Ikura M., Ungrin M., and Meyn M.S. The Bloom syndrome helicase BLM interacts with TRF2 in ALT cells and promotes telomeric DNA synthesis. Hum. Mol. Genet. 11 (2002) 3135-3144
25. Johnson F.B., Marciniak R.A., McVey M., Stewart S.A., Hahn W.C., and Guarente L. The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO J. 20 (2001) 905-913
26. Zhu X.D., Kuster B., Mann M., Petrini J.H., and Lange T. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25 (2000) 347-352
27. Tarsounas M., Munoz P., Claas A., Smiraldo P.G., Pittman D.L., Blasco M.A., and West S.C. Telomere maintenance requires the RAD51D recombination/repair protein. Cell 117 (2004) 337-347
28. Nabetani A., Yokoyama O., and Ishikawa F. Localization of hRad9, hHus1, hRad1, and hRad17 and Caffeine-sensitive DNA Replication at the Alternative Lengthening of Telomeres-associated Promyelocytic Leukemia Body. J. Biol. Chem 279 (2004) 25849-25857
29. Grobelny J.V., Godwin A.K., and Broccoli D. ALT-associated PML bodies are present in viable cells and are enriched in cells in the G(2)/M phase of the cell cycle. J. Cell Sci. 113 (2000) 4577-4585
30. Wu G., Jiang X., Lee W.H., and Chen P.L. Assembly of functional ALT-associated promyelocytic leukemia bodies requires Nijmegen Breakage Syndrome 1. Cancer Res. 63 (2003) 2589-2595
31. Molenaar C., Wiesmeijer K., Verwoerd N.P., Khazen S., Eils R., Tanke H.J., and Dirks R.W. Visualizing telomere dynamics in living mammalian cells using PNA probes. EMBO J. 22 (2003) 6631-6641
32. Marciniak R.A., Cavazos D., Montellano R., Chen Q., Guarente L., and Johnson F.B. A novel telomere structure in a human alternative lengthening of telomeres cell line. Cancer Res. 65 (2005) 2730-2737
33. Fasching C.L., Bower K., and Reddel R.R. Telomerase-independent telomere length maintenance in the absence of alternative lengthening of telomeres-associated promyelocytic leukemia bodies. Cancer Res. 65 (2005) 2722-2729
34. Cerone M.A., Autexier C., Londono-Vallejo J.A., and Bacchetti S. A human cell line that maintains telomeres in the absence of telomerase and of key markers of ALT. Oncogene 24 (2005) 7893-7901
35. Wu G., Lee W.H., and Chen P.L. 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 (2000) 30618-30622
36. Jiang W.Q., Zhong Z.H., Henson J.D., and Reddel R.R. Identification of candidate alternative lengthening of telomeres genes by methionine restriction and RNA interference. Oncogene 26 (2007) 4635-4647
37. Jiang W.Q., Zhong Z.H., Henson J.D., Neumann A.A., Chang A.C., and Reddel R.R. Suppression of alternative lengthening of telomeres by Sp100-mediated sequestration of the MRE11/RAD50/NBS1 complex. Mol. Cell Biol. 25 (2005) 2708-2721
38. Tokutake Y., Matsumoto T., Watanabe T., Maeda S., Tahara H., Sakamoto S., Niida H., Sugimoto M., Ide T., and Furuichi Y. Extra-chromosomal telomere repeat DNA in telomerase-negative immortalized cell lines. Biochem. Biophys. Res. Commun. 247 (1998) 765-772
39. Cesare A.J., and Griffith J.D. Telomeric DNA in ALT cells is characterized by free telomeric circles and heterogeneous t-loops. Mol. Cell Biol. 24 (2004) 9948-9957
40. Wang R.C., and Smogorzewska A. T. de Lange, Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119 (2004) 355-368
41. Groff-Vindman C., Cesare A.J., Natarajan S., Griffith J.D., and McEachern M.J. Recombination at long mutant telomeres produces tiny single- and double-stranded telomeric circles. Mol. Cell Biol. 25 (2005) 4406-4412
42. Compton S.A., Choi J.H., Cesare A.J., Ozgur S., and Griffith J.D. Xrcc3 and Nbs1 are required for the production of extrachromosomal telomeric circles in human alternative lengthening of telomere cells. Cancer Res. 67 (2007) 1513-1519
43. Horn P.J., and Peterson C.L. Heterochromatin assembly: a new twist on an old model. Chromosome Res. 14 (2006) 83-94
44. Okano M., Xie S., and Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat. Genet. 19 (1998) 219-220
45. Okano M., Bell D.W., Haber D.A., and Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99 (1999) 247-257
46. Li E., Bestor T.H., and Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69 (1992) 915-926
47. Chen T., Ueda Y., Dodge J.E., Wang Z., and Li E. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol. Cell Biol. 23 (2003) 5594-5605
48. Lehnertz B., Ueda Y., Derijck A.A., Braunschweig U., Perez-Burgos L., Kubicek S., Chen T., Li E., Jenuwein T., and Peters A.H. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 13 (2003) 1192-1200
49. Chen T., Tsujimoto N., and Li E. The PWWP domain of Dnmt3a and Dnmt3b is required for directing DNA methylation to the major satellite repeats at pericentric heterochromatin. Mol. Cell Biol. 24 (2004) 9048-9058
50. Dodge J.E., Okano M., Dick F., Tsujimoto N., Chen T., Wang S., Ueda Y., and Dyson N. E. Li, Inactivation of Dnmt3b in mouse embryonic fibroblasts results in DNA hypomethylation, chromosomal instability, and spontaneous immortalization. J. Biol. Chem. 280 (2005) 17986-17991
51. Tommerup H., and Dousmanis A. T. de Lange, Unusual chromatin in human telomeres. Mol. Cell Biol. 14 (1994) 5777-5785
52. Fraga M.F., Ballestar E., Villar-Garea A., Boix-Chornet M., Espada J., Schotta G., Bonaldi T., Haydon C., Ropero S., Petrie K., Iyer N.G., Perez-Rosado A., Calvo E., Lopez J.A., Cano A., Calasanz M.J., Colomer D., Piris M.A., Ahn N., Imhof A., Caldas C., Jenuwein T., and Esteller M. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat. Genet. 37 (2005) 391-400
53. van Overveld P.G., Lemmers R.J., Sandkuijl L.A., Enthoven L., Winokur S.T., Bakels F., Padberg G.W., van Ommen G.J., Frants R.R., and van der Maarel S.M. Hypomethylation of D4Z4 in 4q-linked and non-4q-linked facioscapulohumeral muscular dystrophy. Nat. Genet. 35 (2003) 315-317
54. Jenuwein T., and Allis C.D. Translating the histone code. Science 293 (2001) 1074-1080
55. Lachner M., O'Carroll D., Rea S., Mechtler K., and Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410 (2001) 116-120
56. Makarov V.L., Lejnine S., Bedoyan J., and Langmore J.P. Nucleosomal organization of telomere-specific chromatin in rat. Cell 73 (1993) 775-787
57. Garcia-Cao M., O'Sullivan R., Peters A.H., Jenuwein T., and Blasco M.A. Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat. Genet. 36 (2004) 94-99
58. Gonzalo S., Garcia-Cao M., Fraga M.F., Schotta G., Peters A.H., Cotter S.E., Eguia R., Dean D.C., Esteller M., Jenuwein T., and Blasco M.A. Role of the RB1 family in stabilizing histone methylation at constitutive heterochromatin. Nat. Cell Biol. 7 (2005) 420-428
59. Gonzalo S., Jaco I., Fraga M.F., Chen T., Li E., Esteller M., and Blasco M.A. DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat. Cell Biol. 8 (2006) 416-424
60. Koering C.E., Pollice A., Zibella M.P., Bauwens S., Puisieux A., Brunori M., Brun C., Martins L., Sabatier L., Pulitzer J.F., and Gilson E. Human telomeric position effect is determined by chromosomal context and telomeric chromatin integrity. EMBO Rep. 3 (2002) 1055-1061
61. Garcia-Cao M., Gonzalo S., Dean D., and Blasco M.A. A role for the Rb family of proteins in controlling telomere length. Nat. Genet. 32 (2002) 415-419
62. Gonzalo S., and Blasco M.A. Role of Rb family in the epigenetic definition of chromatin. Cell Cycle 4 (2005) 752-755
63. Grafi G., Ben-Meir H., Avivi Y., Moshe M., Dahan Y., and Zemach A. Histone methylation controls telomerase-independent telomere lengthening in cells undergoing dedifferentiation. Dev. Biol. (2007)
64. Benetti R., Garcia-Cao M., and Blasco M.A. Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat. Genet. 39 (2007) 243-250
65. Atkinson S.P., Hoare S.F., Glasspool R.M., and Keith W.N. Lack of telomerase gene expression in alternative lengthening of telomere cells is associated with chromatin remodeling of the hTR and hTERT gene promoters. Cancer Res. 65 (2005) 7585-7590
66. Fraga M.F., and Esteller M. Towards the human cancer epigenome: a first draft of histone modifications. Cell Cycle 4 (2005) 1377-1381
67. Jones P.A., and Baylin S.B. The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 3 (2002) 415-428
68. Esteller M. Epigenetics provides a new generation of oncogenes and tumour-suppressor genes. Br. J. Cancer 94 (2006) 179-183
69. Chang S., Khoo C.M., Naylor M.L., Maser R.S., and DePinho R.A. Telomere-based crisis: functional differences between telomerase activation and ALT in tumor progression. Genes Dev. 17 (2003) 88-100