HipHop interacts with HOAP and HP1 to protect Drosophila telomeres in a sequence-independent manner

EMBO Journal

Volumn 29, Issue 4, 2010, Pages 819-829

  Gao, Guanjun ^a   Walser, Jean Claude ^b,d   Beaucher, Michelle L ^a   Morciano, Patrizia ^a,c   Wesolowska, Natalia ^a   Chen, Jie ^a   Rong, Yikang S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c UNIVERSITY OF L'AQUILA   (Italy)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Capping complex; Drosophila telomere; Epigenetic mechanism; Telomere maintenance

Indexed keywords

ATM PROTEIN; HETEROCHROMATIN PROTEIN 1; MRE11 PROTEIN; PROTEIN; PROTEIN HIPHOP; PROTEIN HOAP; RAD50 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DNA SEQUENCE; DNA STRUCTURE; DROSOPHILA; EPIGENETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN ISOLATION; TELOMERE;

ANIMALS; BINDING SITES; CELL LINE; CHROMOSOMAL PROTEINS, NON-HISTONE; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; GENES, INSECT; MULTIPROTEIN COMPLEXES; MUTATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RNA INTERFERENCE; TELOMERE;

MAMMALIA;

EID: 77149166008     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.394     Document Type: Article

References (61)

1. Ahmad K, Golic KG (1998) The transmission of fragmented chromosomes in Drosophila melanogaster. Genetics 148: 775-792
2. Baumann P, Cech TR (2001) Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292: 1171-1175
3. Bi X, Srikanta D, Fanti L, Pimpinelli S, Badugu R, Kellum R, Rong YS (2005) Drosophila ATM and ATR checkpoint kinases control partially redundant pathways for telomere maintenance. Proc Natl Acad Sci USA 102: 15167-15172
4. Bi X, Wei SC, Rong YS (2004) Telomere protection without a telomerase; the role of ATM and Mre11 in Drosophila telomere maintenance. Curr Biol 14: 1348-1353
5. Biessmann H, Champion LE, O'Hair M, Ikenaga K, Kasravi B, Mason JM (1992) Frequent transpositions of Drosophila melano-gaster HeT-A transposable elements to receding chromosome ends. EMBO J 11: 4459-4469
6. Blasco MA, Lee HW, Hande MP, Samper E, Lansdorp PM, DePinho RA, Greider CW (1997) Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91: 25-34
7. Cenci G, Rawson RB, Belloni G, Castrillon DH, Tudor M, Petrucci R, Goldberg ML, Wasserman SA, Gatti M (1997) UbcD1, a Drosophila ubiquitin-conjugating enzyme required for proper telomere behavior. Genes Dev 11: 863-875
8. Cenci G, Siriaco G, Raffa GD, Kellum R, Gatti M (2003) The Drosophila HOAP protein is required for telomere capping. Nat Cell Biol 5: 82-84 (Pubitemid 36054334)
9. Ciapponi L, Cenci G, Ducau J, Flores C, Johnson-Schlitz D, Gorski MM, Engels WR, Gatti M (2004) The Drosophila Mre11/Rad50 complex is required to prevent both telomeric fusion and chromosome breakage. Curr Biol 14: 1360-1366
10. Ciapponi L, Cenci G, Gatti M (2006) The Drosophila Nbs protein functions in multiple pathways for the maintenance of genome stability. Genetics 173: 1447-1454
11. Conrad MN, Wright JH, Wolf AJ, Zakian VA (1990) RAP1 protein interacts with yeast telomeres in vivo: overproduction alters telomere structure and decreases chromosome stability. Cell 63: 739-750
12. Diede SJ, Gottschling DE (2001) Exonuclease activity is required for sequence addition and Cdc13p loading at a de novo telomere. Curr Biol 11: 1336-1340
13. Fanti L, Giovinazzo G, Berloco M, Pimpinelli S (1998) The hetero-chromatin protein 1 prevents telomere fusions in Drosophila. Mol Cell 2: 527-538
14. Ferreira MG, Cooper JP (2001) The fission yeast Taz1 protein protects chromosomes from Ku-dependent end-to-end fusions. Mol Cell 7: 55-63
15. Frydrychova RC, Mason JM, Archer TK (2008) HP1 is distributed within distinct chromatin domains at Drosophila telomeres. Genetics 180: 121-131
16. Gao H, Cervantes RB, Mandell EK, Otero JH, Lundblad V (2007) RPA-like proteins mediate yeast telomere function. Nat Struct Mol Biol 14: 208-214
17. Gao G, McMahon C, Chen J, Rong YS (2008) A powerful method combining homologous recombination and site-specific recombination for targeted mutagenesis in Drosophila. Proc Natl Acad Sci USA 105: 13999-14004
18. Goudsouzian LK, Tuzon CT, Zakian VA (2006) S. cerevisiae Tel1p and Mre11p are required for normal levels of Est1p and Est2p telomere association. Mol Cell 24: 603-610
19. Grewal SI, Jia S (2007) Heterochromatin revisited. Nat Rev Genet 8: 35-46
20. Kanoh J, Sadaie M, Urano T, Ishikawa F (2005) Telomere binding protein Taz1 establishes Swi6 heterochromatin independently of RNAi at telomeres. Curr Biol 15: 1808-1819
21. Kern AD, Begun DJ (2008) Recurrent deletion and gene presence/ absence polymorphism: telomere dynamics dominate evolution at the tip of 3L in Drosophila melanogaster and D. simulans. Genetics 179: 1021-1027
22. Komonyi O, Schauer T, Papai G, Deak P, Boros IM (2009) A product of the bicistronic Drosophila melanogaster gene CG31241, which also encodes a trimethylguanosine synthase, plays a role in telomere protection. J Cell Sci 122: 769-774
23. Levis RW (1989) Viable deletions of a telomere from a Drosophila chromosome. Cell 58: 791-801
24. Li B, Oestreich S, de Lange T (2000) Identification of human Rap1: implications for telomere evolution. Cell 101: 471-483
25. Liu D, O'Connor MS, Qin J, Songyang Z (2004) Telosome, a mammalian telomere-associated complex formed by multiple telomeric proteins. J Biol Chem 279: 51338-51342
26. Lydall D (2009) Taming the tiger by the tail: modulation of DNA damage responses by telomeres. EMBO J 28: 2174-2187
27. Marcand S, Gilson E, Shore D (1997) A protein-counting mechanism for telomere length regulation in yeast. Science 275: 986-990 (Pubitemid 27087716)
28. Makarov VL, Lejnine S, Bedoyan J, Langmore JP (1993) Nucleosomal organization of telomere-specific chromatin in rat. Cell 73: 775-787
29. Maringele L, Lydall D (2004) Telomerase-and recombination-independent immortalization of budding yeast. Genes Dev 18: 2663-2675
30. Mart́in V, Du LL, Rozenzhak S, Russell P (2007) Protection of telomeres by a conserved Stn1-Ten1 complex. Proc Natl Acad Sci USA 104: 14038-14043
31. Meier B, Clejan I, Liu Y, Lowden M, Gartner A, Hodgkin J, Ahmed S (2006) trt-1 is the Caenorhabditis elegans catalytic subunit of telomerase. PLoS Genet 2: e18
32. Miyoshi T, Kanoh J, Saito M, Ishikawa F (2008) Fission yeast Pot1-Tpp1 protects telomeres and regulates telomere length. Science 320: 1341-1344
33. Negrini S, Ribaud V, Bianchi A, Shore D (2007) DNA breaks are masked by multiple Rap1 binding in yeast: implications for telomere capping and telomerase regulation. Genes Dev 21: 292-302
34. Oikemus SR, Queiroz-Machado J, Lai K, McGinnis N, Sunkel C, Brodsky MH (2006) Epigenetic telomere protection by Drosophila DNA damage response pathways. PLoS Genet 2: e71
35. Pardo B, Marcand S (2005) Rap1 prevents telomere fusions by nonhomologous end joining. EMBO J 24: 3117-3127
36. Pardue ML, Debaryshe PG (2008) Drosophila telomeres: a variation on the telomerase theme. Fly 2: 101-110
37. Perrini B, Piacentini L, Fanti L, Altieri F, Chichiarelli S, Berloco M, Turano C, Ferraro A, Pimpinelli S (2004) HP1 controls telomere capping, telomere elongation, and telomere silencing by two different mechanisms in Drosophila. Mol Cell 15: 467-476
38. Raffa GD, Cenci G, Siriaco G, Goldberg ML, Gatti M (2005) The putative Drosophila transcription factor woc is required to prevent telomeric fusions. Mol Cell 20: 821-831
39. Raffa GD, Siriaco G, Cugusi S, Ciapponi L, Cenci G, Wojcik E, Gatti M (2009) The Drosophila modigliani (moi) gene encodes a HOAP-interacting protein required for telomere protection. Proc Natl Acad Sci USA 106: 2271-2276
40. Rashkova S, Karam SE, Kellum R, Pardue ML (2002) Gag proteins of the two Drosophila telomeric retrotransposons are targeted to chromosome ends. J Cell Biol 159: 397-402
41. Riha K, McKnight TD, Griffing LR, Shippen DE (2001) Living with genome instability: plant responses to telomere dysfunction. Science 291: 1797-1800
42. Rogers SL, Rogers GC (2008) Culture of Drosophila S2 cells and their use for RNAi-mediated loss-of-function studies and immuno-fluorescence microscopy. Nat Protoc 3: 606-611
43. Rong YS, Golic KG (2003) The homologous chromosome is an effective template for the repair of mitotic DNA double-strand breaks in Drosophila. Genetics 165: 1831-1842
44. Rong YS (2008b) Loss of the histone variant H2A.Z restores capping to checkpoint-defective telomeres in Drosophila. Genetics 180: 1869-1875
45. Rong YS (2008a) Telomere capping in Drosophila: dealing with chromosome ends that most resemble DNA breaks. Chromosoma 117: 235-242
46. Schmid KJ, Tautz D (1997) A screen for fast evolving genes from Drosophila. Proc Natl Acad Sci USA 94: 9746-9750
47. Shakirov EV, McKnight TD, Shippen DE (2009) POT1-independent single-strand telomeric DNA-binding activities in Brassicaceae. Plant J 58: 1004-1015
48. Shareef MM, King C, Damaj M, Badagu R, Huang DW, Kellum R (2001) Drosophila heterochromatin protein 1 (HP1)/origin recognition complex (ORC) protein is associated with HP1 and ORC and functions in heterochromatin-induced silencing. Mol Biol Cell 12: 1671-1685
49. Siriaco GM, Cenci G, Haoudi A, Champion LE, Zhou C, Gatti M, Mason JM (2002) Telomere elongation (Tel), a new mutation in Drosophila melanogaster that produces long telomeres. Genetics 160: 235-245
50. Somma MP, Ceprani F, Bucciarelli E, Naim V, De Arcangelis V, Piergentili R, Palena A, Ciapponi L, Giansanti MG, Pellacani C, Petrucci R, Cenci G, Verǹi F, Fasulo B, Goldberg ML, Di Cunto F, Gatti M (2008) Identification of Drosophila mitotic genes by combining co-expression analysis and RNA interference. PLoS Genet 4: e1000126
51. Song X, Leehy K, Warrington RT, Lamb JC, Surovtseva YV, Shippen DE (2008) STN1 protects chromosome ends in Arabidopsis thaliana. Proc Natl Acad Sci USA 105: 19815-19820
52. Strahl-Bolsinger S, Hecht A, Luo K, Grunstein M (1997) SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes Dev 11: 83-93
53. Tommerup H, Dousmanis A, de Lange T (1994) Unusual chromatin in human telomeres. Mol Cell Biol 14: 5777-5785
54. Török T, Benitez C, Takács S, Biessmann H (2007) The protein encoded by the gene proliferation disrupter (prod) is associated with the telomeric retrotransposon array in Drosophila melano-gaster. Chromosoma 116: 185-195
55. van Steensel B, Smogorzewska A, de Lange T (1998) TRF2 protects human telomeres from end-to-end fusions. Cell 92: 401-413
56. Villasante A, de Pablos B, Méndez-Lago M, Abad JP (2008) Telomere maintenance in Drosophila: rapid transposon evolution at chromosome ends. Cell Cycle 7: 2134-2138
57. Watson JM, Bulankova P, Riha K, Shippen DE, Vyskot B (2005) Telomerase-independent cell survival in Arabidopsis thaliana. Plant J 43: 662-674
58. Wei Q, Marchler G, Edington K, Karsch-Mizrachi I, Paterson BM (2000) RNA interference demonstrates a role for nautilus in the myogenic conversion of Schneider cells by daughterless. Dev Biol 228: 239-255
59. Wright JH, Gottschling DE, Zakian VA (1992) Saccharomyces telomeres assume a non-nucleosomal chromatin structure. Genes Dev 6: 197-210
60. Yang Z, Nielsen R (2000) Estimating synonymous and nonsynon-ymous substitution rates under realistic evolutionary models. Mol Biol Evol 17: 32-43
61. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591