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Telomere capping in Drosophila: dealing with chromosome ends that most resemble DNA breaks

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Abstract

Telomere caps prevent chromosome ends from being recognized as DNA double-strand breaks (DSBs). Unlike most organisms studied, the telomere-capping function of Drosophila does not require a specific sequence. Without this sequence component, Drosophila telomeres most resemble DNA breaks and, thus, represent a simpler system for the study of telomere capping. I review recent progress in Drosophila telomere studies, and challenge the notion that Drosophila may not be a relevant model for the study of telomere maintenance.

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References

  • Ahmad K, Golic KG (1998) The transmission of fragmented chromosomes in Drosophila melanogaster. Genetics 148(2):775–792

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmad K, Golic KG (1999) Telomere loss in somatic cells of Drosophila causes cell cycle arrest and apoptosis. Genetics 151(3):1041–1051

    CAS  PubMed  PubMed Central  Google Scholar 

  • Andreyeva EN, Belyaeva ES, Semeshin VF, Pokholkova GV, Zhimulev IF (2005) Three distinct chromatin domains in telomere ends of polytene chromosomes in Drosophila melanogaster Tel mutants. J Cell Sci 118:5465–5477

    Article  CAS  PubMed  Google Scholar 

  • Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, Collins F, Shiloh Y, Crawley JN, Ried T, Tagle D, Wynshaw-Boris A (1996) Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86(1):159–171

    Article  CAS  PubMed  Google Scholar 

  • 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(15):1348–1353

    Article  CAS  PubMed  Google Scholar 

  • Bi X, Srikanta D, Fanti L, Pimpinelli S, Badugu R, Kellum R, Rong YS (2005a) Drosophila ATM and ATR checkpoint kinases control partially redundant pathways for telomere maintenance. Proc Natl Acad Sci U S A 102(42):15167–15172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bi X, Gong M, Srikanta D, Rong YS (2005b) Drosophila ATM and Mre11 are essential for the G2/M checkpoint induced by low-dose irradiation. Genetics 171(2):845–847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biessmann H, Mason JM (1988) Progressive loss of DNA sequences from terminal chromosome deficiencies in Drosophila melanogaster. EMBO J 7(4):1081–1086

    CAS  PubMed  PubMed Central  Google Scholar 

  • Biessmann H, Mason JM (2003) Telomerase-independent mechanisms of telomere elongation. Cell Mol Life Sci 60(11):2325–2333

    Article  CAS  PubMed  Google Scholar 

  • Biessmann H, Carter SB, Mason JM (1990) Chromosome ends in Drosophila without telomeric DNA sequences. Proc Natl Acad Sci U S A 87(5):1758–1761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biessmann H, Champion LE, O’Hair M, Ikenaga K, Kasravi B, Mason JM (1992) Frequent transpositions of Drosophila melanogaster HeT-A transposable elements to receding chromosome ends. EMBO J 11(12):4459–4469

    CAS  PubMed  PubMed Central  Google Scholar 

  • Biessmann H, Kasravi B, Jakes K, Bui T, Ikenaga K, Mason JM (1993) The genomic organization of HeT-A retroposons in Drosophila melanogaster. Chromosoma 102(5):297–305

    Article  CAS  PubMed  Google Scholar 

  • 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(7):863–875

    Article  CAS  PubMed  Google Scholar 

  • Cenci G, Siriaco G, Raffa GD, Kellum R, Gatti M (2003) The Drosophila HOAP protein is required for telomere capping. Nat Cell Biol 5(1):82–84

    Article  CAS  PubMed  Google Scholar 

  • Cenci G, Ciapponi L, Gatti M (2005) The mechanism of telomere protection: a comparison between Drosophila and humans. Chromosoma 114(3):135–145

    Article  CAS  PubMed  Google Scholar 

  • Chan SW, Blackburn EH (2003) Telomerase and ATM/Tel1p protect telomeres from nonhomologous end joining. Mol Cell 11:1379–1387

    Article  CAS  PubMed  Google Scholar 

  • Chin GM, Villeneuve AM (2001) C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G(2) DNA damage checkpoint. Genes Dev 15(5):522–534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(15):1360–1366

    Article  CAS  PubMed  Google Scholar 

  • Ciapponi L, Cenci G, Gatti M (2006) The Drosophila Nbs protein functions in multiple pathways for the maintenance of genome stability. Genetics 173(3):1447–1454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costanzo V, Robertson K, Bibikova M, Kim E, Grieco D, Gottesman M, Carroll D, Gautier J (2001) Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol Cell 8(1):137–147

    Article  CAS  PubMed  Google Scholar 

  • Daoudal-Cotterell S, Gallego ME, White CI (2002) The plant Rad50-Mre11 protein complex. FEBS Lett 516(1–3):164–166

    Article  CAS  PubMed  Google Scholar 

  • de Lange T (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19(18):2100–2110

    Article  PubMed  Google Scholar 

  • Fanti L, Giovinazzo G, Berloco M, Pimpinelli S (1998) The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol Cell 2(5):527–538

    Article  CAS  PubMed  Google Scholar 

  • Garcia V, Bruchet H, Camescasse D, Granier F, Bouchez D, Tissier A (2003) AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15(1):119–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao LY, Armanios M, Strong MA, Karim B, Feldser DM, Huso D, Greider CW (2005) Short telomeres, even in the presence of telomerase, limit tissue renewal capacity. Cell 123(6):1121–1131

    Article  CAS  PubMed  Google Scholar 

  • Heacock M, Spangler E, Riha K, Puizina J, Shippen DE (2004) Molecular analysis of telomere fusions in Arabidopsis: multiple pathways for chromosome end-joining. EMBO J 23(11):2304–2313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heacock ML, Idol RA, Friesner JD, Britt AB, Shippen DE (2007) Telomere dynamics and fusion of critically shortened telomeres in plants lacking DNA ligase IV. Nucleic Acids Res, Sep 25; [Epub ahead of print]

  • Levis RW (1989) Viable deletions of a telomere from a Drosophila chromosome. Cell 58(4):791–801

    Article  CAS  PubMed  Google Scholar 

  • Maringele L, Lydall D (2004) Telomerase- and recombination-independent immortalization of budding yeast. Genes Dev 18:2663–2675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McClintock B (1939) The Behavior in Successive Nuclear Divisions of a Chromosome Broken at Meiosis. Proc Natl Acad Sci U S A 25(8):405–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McEachern MJ, Krauskopf A, Blackburn EH (2000) Telomeres and their control. Annu Rev Genet 34:331–358

    Article  CAS  PubMed  Google Scholar 

  • Melnikova L, Georgiev P (2005) Drosophila telomeres: the non-telomerase alternative. Chromosome Res 13(5):431–441

    Article  CAS  PubMed  Google Scholar 

  • Mieczkowski PA, Mieczkowska JO, Dominska M, Petes TD (2003) Genetic regulation of telomere-telomere fusions in the yeast Saccharomyces cerevisae. Proc Natl Acad Sci U S A 100(19):10854–10859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mikhailovsky S, Belenkaya T, Georgiev P (1999) Broken chromosomal ends can be elongated by conversion in Drosophila melanogaster. Chromosoma 108(2):114–120

    Article  CAS  PubMed  Google Scholar 

  • Nakamura TM, Moser BA, Russell P (2002) Telomere binding of checkpoint sensor and DNA repair proteins contributes to maintenance of functional fission yeast telomeres. Genetics 161(4):1437–1452

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pardue ML, DeBaryshe PG (2003) Retrotransposons provide an evolutionarily robust non-telomerase mechanism to maintain telomeres. Annu Rev Genet 37:485–511

    Article  CAS  PubMed  Google Scholar 

  • 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(3):467–476

    Article  CAS  PubMed  Google Scholar 

  • Oikemus SR, McGinnis N, Queiroz-Machado J, Tukachinsky H, Takada S, Sunkel CE, Brodsky MH (2004) Drosophila atm/telomere fusion is required for telomeric localization of HP1 and telomere position effect. Genes Dev 18(15):1850–1861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(5):e71

    Article  PubMed  PubMed Central  Google Scholar 

  • Qi L, Strong MA, Karim BO, Armanios M, Huso DL, Greider CW (2003) Short telomeres and ataxia-telangiectasia mutated deficiency cooperatively increase telomere dysfunction and suppress tumorigenesis. Cancer Res 63(23):8188–8196

    CAS  PubMed  Google Scholar 

  • 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(6):821–831

    Article  CAS  PubMed  Google Scholar 

  • Reddel RR (2003) Alternative lengthening of telomeres, telomerase, and cancer. Cancer Lett 194(2):155–162

    Article  CAS  PubMed  Google Scholar 

  • Ritchie KB, Mallory JC, Petes TD (1999) Interactions of TLC1 (which encodes the RNA subunit of telomerase), TEL1, and MEC1 in regulating telomere length in the yeast Saccharomyces cerevisiae. Mol Cell Biol 19:6065–6075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savitsky K, Bar-Shira A, Gilad S, Rotman G, Ziv Y, Vanagaite L, Tagle DA, Smith S, Uziel T, Sfez S, Ashkenazi M, Pecker I, Frydman M, Harnik R, Patanjali SR, Simmons A, Clines GA, Sartiel A, Gatti RA, Chessa L, Sanal O, Lavin MF, Jaspers NG, Taylor AM, Arlett CF, Miki T, Weissman SM, Lovett M, Collins FS, Shiloh Y (1995) A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268(5218):1749–1753

    Article  CAS  PubMed  Google Scholar 

  • 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(6):1671–1685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva E, Tiong S, Pedersen M, Homola E, Royou A, Fasulo B, Siriaco G, Campbell SD (2004) ATM is required for telomere maintenance and chromosome stability during Drosophila development. Curr Biol 14(15):1341–1347

    Article  CAS  PubMed  Google Scholar 

  • Song YH, Mirey G, Betson M, Haber DA, Settleman J (2004) The Drosophila ATM ortholog, dATM, mediates the response to ionizing radiation and to spontaneous DNA damage during development. Curr Biol 14(15):1354–1359

    Article  CAS  PubMed  Google Scholar 

  • Takata H, Kanoh Y, Gunge N, Shirahige K, Matsuura A (2004) Reciprocal association of the budding yeast ATM-related proteins Tel1 and Mec1 with telomeres in vivo. Mol Cell 14(4):515–522

    Article  CAS  PubMed  Google Scholar 

  • Teixeira MT, Arneric M, Sperisen P, Lingner J (2004) Telomere length homeostasis is achieved via a switch between telomerase- extendible and -nonextendible states. Cell 117:323–335

    Article  CAS  PubMed  Google Scholar 

  • 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 melanogaster. Chromosoma 116(2):185–195

    Article  PubMed  Google Scholar 

  • Vespa L, Couvillion M, Spangler E, Shippen DE (2005) ATM and ATR make distinct contributions to chromosome end protection and the maintenance of telomeric DNA in Arabidopsis. Genes Dev 19:2111–2115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waterworth WM, Altun C, Armstrong SJ, Roberts N, Dean PJ, Young K, Weil CF, Bray CM, West CE (2007) NBS1 is involved in DNA repair and plays a synergistic role with ATM in mediating meiotic homologous recombination in plants. Plant J 52(1):41–52

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Iwai Y, Sonoda E, Sasaki MS, Morrison C, Haraguchi T, Hiraoka Y, Yamashita YM, Yagi T, Takata M, Price C, Kakazu N, Takeda S (1999) Mre11 is essential for the maintenance of chromosomal DNA in vertebrate cells. EMBO J 18(23):6619–6629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zubko MK, Lydall D (2006) Linear chromosome maintenance in the absence of essential telomere-capping proteins. Nat Cell Biol 8(7):734–740

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

I thank Dr. Michael Lichten and Conor McMahon at NCI, and Dr. Rebecca Kellum at University of Kentucky for comments on the review. Research in my group is supported by the Intramural Program of the National Cancer Institute.

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Authors and Affiliations

  1. Laboratory of Biochemistry and Molecular Biology, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, 20892, USA

    Yikang S. Rong

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Correspondence to Yikang S. Rong.

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Communicated by S. Pimpinelli

This review article is part of a series dedicated to the eighth International conference on Drosophila heterochromatin, held in Gubbio (Italy), June 2007.

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Rong, Y.S. Telomere capping in Drosophila: dealing with chromosome ends that most resemble DNA breaks. Chromosoma 117, 235–242 (2008). https://doi.org/10.1007/s00412-007-0144-2

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  • DOI: https://doi.org/10.1007/s00412-007-0144-2

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