Organization and evolution of Drosophila terminin: Similarities and differences between Drosophila and human telomeres

Frontiers in Oncology

Volumn 3 MAY, Issue , 2013, Pages

  Raffa, Grazia D ^a   Cenci, Giovanni ^a   Ciapponi, Laura ^a   Gatti, Maurizio ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Drosophila; Non terminin proteins; Telomere fusion; Telomere protection; Terminin

Indexed keywords

DROSOPHILA PROTEIN; HETEROCHROMATIN PROTEIN 1; RAD50 PROTEIN; SHELTERIN; TELOMERASE; TELOMERIC REPEAT BINDING FACTOR 1; TELOMERIC REPEAT BINDING FACTOR 2; TERMININ; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

EPIGENETICS; GENE; GENETIC DIFFERENCE; GENETIC SIMILARITY; HUMAN; MOLECULAR GENETICS; NONHUMAN; REVIEW; TELOMERE; TELOMERE CAPPING; TELOMERE HOMEOSTASIS;

EID: 84887471653     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00112     Document Type: Review

References (60)

1. Ahmad, K., and Golic, K. G. (1998). The transmission of fragmented chromosomes in Drosophila melanogaster. Genetics 148, 775-792.
2. Beaucher, M., Zheng, X. F., Amariei, F., and Rong, Y. S. (2012). Multiple pathways suppress telomere addition to DNA breaks in the Drosophila germline. Genetics 191, 407-417.
3. Bi, X., Srikanta, D., Fanti, L., Pimpinelli, S., Badugu, R., Kellum, R., et al. (2005). Drosophila ATM and ATR checkpoint kinases control partially redundant pathways for telomere maintenance. Proc. Natl. Acad. Sci. U.S.A. 102, 15167-15172.
4. Bi, X., Wei, S. D., and Rong, Y. S. (2004). Telomere protection without a telomerase: the role of ATM and Mre11 in Drosophila telomere maintenance. Curr. Biol. 14, 1348-1353.
5. Biessmann, H., Carter, S. B., and Mason, J. M. (1990). Chromosome ends in Drosophila without telomeric DNA sequences. Proc. Natl. Acad. Sci. U.S.A. 87, 1758-1761.
6. Biessmann, H., and Mason, J. M. (1988). Progressive loss of DNA sequences from terminal chromosome deficiencies in Drosophila melanogaster. EMBO J. 7, 1081-1086.
7. Capkova Frydrychova, R., Biessmann, H., and Mason, J. M. (2008). Regulation of telomere length in Drosophila. Cytogenet. Genome Res. 122, 356-364.
8. Cenci, G. (2009). Drosophila cell cycle under arrest: uncapped telomeres plead guilty. Cell Cycle 8, 990-995.
9. Cenci, G., Ciapponi, L., and Gatti, M. (2005). The mechanism of telomere protection: a comparison between Drosophila and humans. Chromosoma 114, 135-145.
10. Cenci, G., Rawson, R. B., Belloni, G., Castrillon, D. H., Tudor, M., Petrucci, R., et al. (1997). UbcD1, a Drosophila ubiquitin-conjugating enzyme required for proper telomere behavior. Genes Dev. 11, 863-875.
11. Cenci, G., Siriaco, G., Raffa, G. D., Kellum, R., and Gatti, M. (2003). The Drosophila HOAP protein is required for telomere capping. Nat. Cell Biol. 5, 82-84.
12. Chiolo, I., Minoda, A., Colmenares, S. U., Polyzos, A., Costes, S. V., and Karpen, G. H. (2010). Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144, 732-744.
13. Ciapponi, L., and Cenci, G. (2008). Telomere capping and cellular checkpoints: clues from fruit flies. Cytogenet. Genome Res. 122, 365-373.
14. Ciapponi, L., Cenci, G., Ducau, J., Flores, C., Johnson-Schlitz, D., Gorsky, M. M., et al. (2004). The Drosophila Mre11/Rad50 Complex is required to prevent both telomeric fusion and chromosome breakage. Curr. Biol. 14, 1360-1366.
15. Ciapponi, L., Cenci, G., and Gatti, M. (2006). The Drosophila Nbs protein functions in multiple pathways for the maintenance of genome stability. Genetics 173, 1447-1454.
16. Dronamraju, R., and Mason, J. M. (2009). Recognition of double strand breaks by a mutator protein (MU2) in Drosophila melanogaster. PLoS Genet. 5:e1000473. doi:10.1371/journal.pgen.1000473
17. Fanti, L., Giovinazzo, G., Berloco, M., and Pimpinelli, S. (1998). The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol. Cell 2, 527-538.
18. Fanti, L., and Pimpinelli, S. (2008). HP1: a functionally multifaceted protein. Curr. Opin. Genet. Dev. 18, 169-174.
19. Filion, G. J., Van Bemmel, J. G., Braunschweig, U., Talhout, W., Kind, J., Ward, L. D., et al. (2011). Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143, 212-224.
20. Font-Burgada, J., Rossell, D., Auer, H., and Azorin, F. (2008). Drosophila HP1c isoform interacts with the zinc-finger proteins WOC and Relative-of-WOC to regulate gene expression. Genes Dev. 22, 3007-3023.
21. Gao, G., Walser, J. C., Beaucher, M. L., Morciano, P., Wesolowska, N., Chen, J., et al. (2010). HipHop interacts with HOAP and HP1 to protect Drosophila telomeres in a sequence-independent manner. EMBO J. 29, 819-829.
22. Gu, P., Min, J. N., Wang, Y., Huang, C., Peng, T., Chai, W., et al. (2012). CTC1 deletion results in defective telomere replication, leading to catastrophic telomere loss and stem cell exhaustion. EMBO J. 31, 2309-2321.
23. Jain, D., and Cooper, J. P. (2010). Telomeric strategies: means to an end. Annu. Rev. Genet. 44, 243-269.
24. Martinez, P., Thanasoula, M., Munoz, P., Liao, C., Tejera, A., McNees, C., et al. (2009). Increased telomere fragility and fusions resulting from TRF1 deficiency lead to degenerative pathologies and increased cancer in mice. Genes Dev. 23, 2060-2075.
25. Mason, J. M., Frydrychova, R. C., and Biessmann, H. (2008). Drosophila telomeres: an exception providing new insights. Bioessays 30, 25-37.
26. Melnikova, L., Biessmann, H., and Georgiev, P. (2005). The Ku protein complex is involved in length regulation of Drosophila telomeres. Genetics 170, 221-235.
27. Melnikova, L., and Georgiev, P. (2002). Enhancer of terminal gene conversion, a new mutation in Drosophila melanogaster that induces telomere elongation by gene conversion. Genetics 162, 1301-1312.
28. Muller, H. J. (1938). The remaking of chromosomes. Collect. Net 8, 182-195.
29. Muñoz, P., Blanco, R., De Carcer, G., Schoeftner, S., Benetti, R., Flores, J. M., et al. (2009). TRF1 controls telomere length and mitotic fidelity in epithelial homeostasis. Mol. Cell. Biol. 29, 1608-1625.
30. Musarò, M., Ciapponi, L., Fasulo, B., Gatti, M., and Cenci, G. (2008). Unprotected Drosophila melanogaster telomeres activate the spindle assembly checkpoint. Nat. Genet. 40, 362-366.
31. Oikemus, S. R., McGinnis, N., Queiroz-Machado, J., Tukachinsky, H., Takada, S., Sunkel, C. E., et al. (2004). Drosophila atm/telomere fusion is required for telomeric localization of HP1 and telomere position effect. Genes Dev. 18, 1850-1861.
32. Oikemus, S. R., Queiroz-Machado, J., Lai, K., McGinnis, N., Sunkel, C., and Brodsky, M. H. (2006). Epigenetic telomere protection by Drosophila DNA damage response pathways. PLoS Genet. 2:e71. doi:10.1371/journal.pgen.0020071
33. O'Sullivan, R. J., and Karlseder, J. (2010). Telomeres: protecting chromosomes against genome instability. Nat. Rev. Mol. Cell Biol. 11, 171-181.
34. Palm, W., and de Lange, T. (2008). How shelterin protects mammalian telomeres. Annu. Rev. Genet. 42, 301-334.
35. Pardue, M. L., and Debaryshe, P. G. (2011). Retrotransposons that maintain chromosome ends. Proc. Natl. Acad. Sci. U.S.A. 108, 20317-20324.
36. Perrini, B., Piacentini, L., Fanti, L., Altieri, F., Chichiarelli, S., Berloco, M., et al. (2004). HP1 controls telomere capping, telomere elongation, and telomere silencing by two different mechanisms in Drosophila. Mol. Cell 15, 467-476.
37. Piacentini, L., Fanti, L., Negri, R., Del Vescovo, V., Fatica, A., Altieri, F., et al. (2009). Heterochromatin protein 1 (HP1a) positively regulates euchromatic gene expression through RNA transcript association and interaction with hnRNPs in Drosophila. PLoS Genet. 5:e1000670. doi:10.1371/journal.pgen.1000670
38. Raffa, G. D., Cenci, G., Siriaco, G., Goldberg, M. L., and Gatti, M. (2005). The putative Drosophila transcription factor woc is required to prevent telomeric fusions. Mol. Cell 20, 821-831.
39. Raffa, G. D., Ciapponi, L., Cenci, G., and Gatti, M. (2011). Terminin: a protein complex that mediates epigenetic maintenance of Drosophila telomeres. Nucleus 2, 383-391.
40. Raffa, G. D., Raimondo, D., Sorino, C., Cugusi, S., Cenci, G., Cacchione, S., et al. (2010). Verrocchio, a Drosophila OB fold-containing protein, is a component of the terminin telomere-capping complex. Genes Dev. 24, 1596-1601.
41. Raffa, G. D., Siriaco, G., Cugusi, S., Ciapponi, L., Cenci, G., Wojcik, E., et al. (2009). The Drosophila modigliani (moi) gene encodes a HOAP-interacting protein required for telomere protection. Proc. Natl. Acad. Sci. U.S.A. 106, 2271-2276.
42. Rong, Y. S. (2008). Telomere capping in Drosophila: dealing with chromosome ends that most resemble DNA breaks. Chromosoma 117, 235-242.
43. Savitsky, M., Kravchuk, O., Melnikova, L., and Georgiev, P. (2002). Heterochromatin protein 1 is involved in control of telomere elongation in Drosophila melanogaster. Mol. Cell. Biol. 22, 3204-3218.
44. Savitsky, M., Kwon, D., Georgiev, P., Kalmykova, A., and Gvozdev, V. (2006). Telomere elongation is under the control of the RNAi-based mechanism in the Drosophila germline. Genes Dev. 20, 345-354.
45. Sfeir, A., and de Lange, T. (2012). Removal of shelterin reveals the telomere end-protection problem. Science 336, 593-597.
46. Sfeir, A., Kosiyatrakul, S. T., Hockemeyer, D., MacRae, S. L., Karlseder, J., Schildkraut, C. L., et al. (2009). Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138, 90-103.
47. Shpiz, S., Olovnikov, I., Sergeeva, A., Lavrov, S., Abramov, Y., Savitsky, M., et al. (2011). Mechanism of the piRNA-mediated silencing of Drosophila telomeric retrotransposons. Nucleic Acids Res. 39, 8703-8711.
48. Silva, E., Tiong, S., Pedersen, M., Homola, E. M., Royou, A., Fasulo, B., et al. (2004). ATM is required for telomere maintenance and chromosome stability during Drosophila development. Curr. Biol. 14, 1341-1347.
49. Silva-Sousa, R., Lopez-Panades, E., Pineyro, D., and Casacuberta, E. (2012). The chromosomal proteins JIL-1 and Z4/Putzig regulate the telomeric chromatin in Drosophila melanogaster. PLoS Genet. 8:e1003153. doi:10.1371/journal.pgen.1003153
50. Siriaco, G. M., Cenci, G., Haoudi, A., Champion, L. E., Zhou, C., Gatti, M., et al. (2002). Telomere elongation (Tel), a new mutation in Drosophila melanogaster that produces long telomeres. Genetics 160, 235-245.
51. Song, Y. H., Mirey, G., Betson, M., Haber, D. A., and Settleman, J. (2004). The Drosophila ATM ortholog, dATM, mediates the response to ionizing radiation and to spontaneous DNA damage during development. Curr. Biol. 14, 1354-1359.
52. Stewart, J. A., Wang, F., Chaiken, M. F., Kasbek, C., Chastain, P. D. III, Wright, W. E., et al. (2012). Human CST promotes telomere duplex replication and general replication restart after fork stalling. EMBO J. 31, 3537-3549.
53. Titen, S. W., and Golic, K. G. (2010). Healing of euchromatic chromosome breaks by efficient de novo telomere addition in Drosophila melanogaster. Genetics 184, 309-312.
54. Török, T., Benitez, C., Takacs, S., and Biessmann, H. (2007). The protein encoded by the gene proliferation disrupter (prod) is associated with the telomeric retrotransposon array in Drosophila melanogaster. Chromosoma 116, 185-195.
55. Tower, J., Karpen, G. H., Craig, N., and Spradling, A. C. (1993). Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics 133, 347-359.
56. Vannier, J. B., Pavicic-Kaltenbrunner, V., Petalcorin, M. I., Ding, H., and Boulton, S. J. (2012). RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 149, 795-806.
57. Vermaak, D., and Malik, H. S. (2009). Multiple roles for heterochromatin protein 1 genes in Drosophila. Annu. Rev. Genet. 43, 467-492.
58. Wang, F., Stewart, J. A., Kasbek, C., Zhao, Y., Wright, W. E., and Price, C. M. (2012). Human CST has independent functions during telomere duplex replication and C-strand fill-in. Cell Rep. 2, 1096-1103.
59. Ye, J., Lenain, C., Bauwens, S., Rizzo, A., Saint-Leger, A., Poulet, A., et al. (2010). TRF2 and apollo cooperate with topoisomerase 2alpha to protect human telomeres from replicative damage. Cell 142, 230-242.
60. Zhang, L., and Rong, Y. S. (2012). Retrotransposons at Drosophila telomeres: host domestication of a selfish element for the maintenance of genome integrity. Biochim. Biophys. Acta 1819, 771-775.