Telomere elongation chooses TERRA ALTernatives

RNA Biology

Volumn 12, Issue 9, 2015, Pages 938-941

  Arora, Rajika ^a   Azzalin, Claus M ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

ALT; RNA:DNA hybrids; RPA; Telomere elongation; Telomere recombination; Telomere transcription; TERRA

Indexed keywords

LONG UNTRANSLATED RNA; PROMYELOCYTIC LEUKEMIA PROTEIN; REPLICATION FACTOR A; RIBONUCLEASE H; SINGLE STRANDED DNA BINDING PROTEIN; TELOMERASE; TELOMERIC REPEAT CONTAINING RNA; UNCLASSIFIED DRUG; PROTEIN BINDING; TELOMERE BINDING PROTEIN;

ALPHA THALASSEMIA; ARTICLE; BASE PAIRING; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DEATH; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CPG ISLAND; DNA DAMAGE; DNA REPAIR; DNA RNA HYBRIDIZATION; DNA STRUCTURE; DOWN REGULATION; ENZYME INACTIVATION; ENZYME REPRESSION; GENETIC TRANSCRIPTION; HOMOLOGOUS RECOMBINATION; HUMAN; NONHUMAN; PROMOTER REGION; PROMYELOCYTIC LEUKEMIA; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SISTER CHROMATID EXCHANGE; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING; U2OS CELL LINE; UPREGULATION; BIOLOGICAL MODEL; GENETICS; METABOLISM;

HOMOLOGOUS RECOMBINATION; HUMANS; MODELS, BIOLOGICAL; PROTEIN BINDING; RNA, LONG NONCODING; TELOMERE HOMEOSTASIS; TELOMERE-BINDING PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84949230728     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.1080/15476286.2015.1065374     Document Type: Article

References (36)

1. Cesare AJ, Reddel RR. Alternative lengthening of telomeres: models, mechanisms and implications. Nat Rev Genet 2010; 11: 319-30; PMID: 20351727; http://dx. doi. org/10. 1038/nrg2763.
2. Conomos D, Pickett HA, Reddel RR. Alternative lengthening of telomeres: remodeling the telomere architecture. Front Oncol 2013; 3: 27; PMID: 23429284; http://dx. doi. org/10. 3389/fonc. 2013. 00027.
3. Draskovic I, Londono-Vallejo A. Telomere recombination and alternative telomere lengthening mechanisms. Front Biosci 2013; 18: 1-20; PMID: 23276906; http://dx. doi. org/10. 2741/4084.
4. Bryan TM, Englezou A, Dalla-Pozza L, DunhamMA, Reddel RR. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumorderived cell lines. Nat Med 1997; 3: 1271-4; PMID: 9359704; http://dx. doi. org/10. 1038/nm1197-1271.
5. Lackner DH, Raices M, Maruyama H, Haggblom C, Karlseder J. Organismal propagation in the absence of a functional telomerase pathway in Caenorhabditis elegans. EMBO J 2012; 31: 2024-33; PMID: 22425786; http://dx. doi. org/10. 1038/emboj. 2012. 61.
6. Hande MP, Samper E, Lansdorp P, Blasco MA. Telomere length dynamics and chromosomal instability in cells derived from telomerase null mice. J Cell Biol 1999; 144: 589-601; PMID: 10037783; http://dx. doi. org/10. 1083/jcb. 144. 4. 589.
7. Le S, Moore JK, Haber JE, Greider CW. RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics 1999; 152: 143-52; PMID: 10224249.
8. O'Hare TH, Delany ME. Molecular and cellular evidence for the alternative lengthening of telomeres (ALT) mechanism in chicken. Cytogenet Genome Res 2011; 135: 65-78; PMID: 21822009; http://dx. doi. org/10. 1159/000330125.
9. Henson JD, Reddel RR. Assaying and investigating Alternative Lengthening of Telomeres activity in human cells and cancers. FEBS Lett 2010; 584: 3800-11; PMID: 20542034; http://dx. doi. org/10. 1016/j. febslet. 2010. 06. 009.
10. Hu J, Hwang SS, Liesa M, Gan B, Sahin E, Jaskelioff M, Ding Z, Ying H, Boutin AT, Zhang H, et al. Antitelomerase therapy provokes ALT and mitochondrial adaptive mechanisms in cancer. Cell 2012; 148: 651-63; PMID: 22341440; http://dx. doi. org/10. 1016/j. cell. 2011. 12. 028.
11. ChenW, Xiao BK, Liu JP, Chen SM, Tao ZZ. Alternative lengthening of telomeres in hTERT-inhibited laryngeal cancer cells. Cancer Sci 2010; 101: 1769-76; PMID: 20545697; http://dx. doi. org/10. 1111/j. 1349-7006. 2010. 01611. x.
12. Lovejoy CA, Li W, Reisenweber S, Thongthip S, Bruno J, de Lange T, De S, Petrini JH, Sung PA, Jasin M, et al. Loss of ATRX, genome instability, and an altered DNA damage response are hallmarks of the alternative lengthening of telomeres pathway. PLoS Genet 2012; 8: e1002772; PMID: 22829774; http://dx. doi. org/10. 1371/journal. pgen. 1002772.
13. Jiang WQ, Zhong ZH, Henson JD, Neumann AA, Chang AC, Reddel RR. Suppression of alternative lengthening of telomeres by Sp100-mediated sequestration of the MRE11/RAD50/NBS1 complex. Mol Cell Biol 2005; 25: 2708-21; PMID: 15767676; http://dx. doi. org/10. 1128/MCB. 25. 7. 2708-2721. 2005.
14. Zhong ZH, Jiang WQ, Cesare AJ, Neumann AA, Wadhwa R, Reddel RR. Disruption of telomere maintenance by depletion of the MRE11/RAD50/NBS1 complex in cells that use alternative lengthening of telomeres. J Biol Chem 2007; 282: 29314-22; PMID: 17693401; http://dx. doi. org/10. 1074/jbc. M701413200.
15. Zeng S, Xiang T, Pandita TK, Gonzalez-Suarez I, Gonzalo S, Harris CC, Yang Q. Telomere recombination requires the MUS81 endonuclease. Nat Cell Biol 2009; 11: 616-23; PMID: 19363487; http://dx. doi. org/10. 1038/ncb1867.
16. Tarsounas M, Muñoz P, Claas A, Smiraldo PG, Pittman DL, Blasco MA, West SC. Telomere maintenance requires the RAD51D recombination/repair protein. Cell 2004; 117: 337-47; PMID: 15109494; http://dx. doi. org/10. 1016/S0092-8674(04)00337-X.
17. Compton SA, Choi JH, Cesare AJ, Ozgur S, Griffith JD. Xrcc3 and Nbs1 are required for the production of extrachromosomal telomeric circles in human alternative lengthening of telomere cells. Cancer Res 2007; 67: 1513-9; PMID: 17308089; http://dx. doi. org/10. 1158/0008-5472. CAN-06-3672.
18. Saharia A, Stewart SA. FEN1 contributes to telomere stability in ALT-positive tumor cells. Oncogene 2008; 28: 1162-7; PMID: 19137021; http://dx. doi. org/10. 1038/onc. 2008. 458.
19. Grudic A, Jul-Larsen A, Haring SJ, Wold MS, Lønning PE, Bjerkvig R, Bøe SO. Replication protein A prevents accumulation of single-stranded telomeric DNA in cells that use alternative lengthening of telomeres. Nucleic Acids Res 2007; 35: 7267-78; PMID: 17959650; http://dx. doi. org/10. 1093/nar/gkm738.
20. Arora R, Brun CM, Azzalin CM. TERRA: long noncoding RNA at eukaryotic telomeres. Prog Mol Subcell Biol 2011; 51: 65-94; PMID: 21287134; http://dx. doi. org/10. 1007/978-3-642-16502-3_4.
21. Azzalin CM, Lingner J. Telomere functions grounding on TERRA firma. Trends Cell Biol 2015; 25: 29-36; PMID: 25257515; http://dx. doi. org/10. 1016/j. tcb. 2014. 08. 007.
22. Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007; 318: 798-801; PMID: 17916692; http://dx. doi. org/10. 1126/science. 1147182.
23. Schoeftner S, Blasco MA. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 2008; 10: 228-36; PMID: 18157120; http://dx. doi. org/10. 1038/ncb1685.
24. Episkopou H, Draskovic I, Van Beneden A, Tilman G, Mattiussi M, Gobin M, Arnoult N, Londoño-Vallejo A, Decottignies A. Alternative Lengthening of Telomeres is characterized by reduced compaction of telomeric chromatin. Nucleic Acids Res 2014; 42: 4391-05; PMID: 24500201; http://dx. doi. org/10. 1093/nar/gku114.
25. Arora R, Lee Y, Wischnewski H, Brun CM, Schwarz T, Azzalin CM. RNaseH1 regulates TERRA-telomeric DNA hybrids and telomere maintenance in ALT tumour cells. Nat Commun 2014; 5: 5220; PMID: 25330849; http://dx. doi. org/10. 1038/ncomms 6220.
26. Nergadze SG, Farnung BO, Wischnewski H, Khoriauli L, Vitelli V, Chawla R, Giulotto E, Azzalin CM. CpGisland promoters drive transcription of human telomeres. RNA 2009; 15: 2186-94; PMID: 19850908; http://dx. doi. org/10. 1261/rna. 1748309.
27. Flynn RL, Cox KE, Jeitany M, Wakimoto H, Bryll AR, Ganem NJ, Bersani F, Pineda JR, Suva ML, Benes CH, et al. Alternative lengthening of telomeres renders cancer cells hypersensitive to ATR inhibitors. Science 2015; 347: 273-7; PMID: 25593184; http://dx. doi. org/10. 1126/science. 1257216.
28. Porro A, Feuerhahn S, Reichenbach P, Lingner J. Molecular dissection of telomeric repeat-containing RNA biogenesis unveils the presence of distinct and multiple regulatory pathways. Mol Cell Biol 2010; 30: 4808-17; PMID: 20713443; http://dx. doi. org/10. 1128/MCB. 00460-10.
29. Balk B, Maicher A, Dees M, Klermund J, Luke-Glaser S, Bender K, Luke B. Telomeric RNA-DNA hybrids affect telomere-length dynamics and senescence. Nat Struct Mol Biol 2013; 20: 1199-205; PMID: 24013207; http://dx. doi. org/10. 1038/nsmb. 2662.
30. Pfeiffer V, Crittin J, Grolimund L, Lingner J. The THO complex component Thp2 counteracts telomeric R-loops and telomere shortening. EMBO J 2013; 32: 2861-71; PMID: 24084588; http://dx. doi. org/10. 1038/emboj. 2013. 217.
31. Yu TY, Kao YW, Lin JJ. Telomeric transcripts stimulate telomere recombination to suppress senescence in cells lacking telomerase. Proc Natl Acad Sci U S A 2014; 111: 3377-82; PMID: 24550456; http://dx. doi. org/10. 1073/pnas. 1307415111.
32. Deng Z, Norseen J, Wiedmer A, Riethman H, Lieberman PM. TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol Cell 2009; 35: 403-13; PMID: 19716786; http://dx. doi. org/10. 1016/j. molcel. 2009. 06. 025.
33. Flynn RL, Centore RC, O'Sullivan RJ, Rai R, Tse A, Songyang Z, Chang S, Karlseder J, Zou L. TERRA and hnRNPA1 orchestrate an RPA-to-POT1 switch on telomeric single-stranded DNA. Nature 2011; 471: 532-6; PMID: 21399625; http://dx. doi. org/10. 1038/nature09772.
34. Renkawitz J, Lademann CA, Kalocsay M, Jentsch S. Monitoring homology search during DNA doublestrand break repair in vivo. Mol Cell 2013; 50: 261-72; PMID: 23523370; http://dx. doi. org/10. 1016/j. molcel. 2013. 02. 020.
35. Cho NW, Dilley RL, Lampson MA, Greenberg RA. Interchromosomal homology searches drive directional ALT telomere movement and synapsis. Cell 2014; 159: 108-21; PMID: 25259924; http://dx. doi. org/10. 1016/j. cell. 2014. 08. 030.
36. Cusanelli E, Romero CA, Chartrand P. Telomeric noncoding RNA TERRA is induced by telomere shortening to nucleate telomerase molecules at short telomeres. Mol Cell 2013; 51: 780-91; PMID: 24074956; http://dx. doi. org/10. 1016/j. molcel. 2013. 08. 029.