The Ku protein complex is involved in length regulation of Drosophila telomeres

Genetics

Volumn 170, Issue 1, 2005, Pages 221-235

  Melnikova, Larisa ^a   Biessmann, Harald ^b   Georgiev, Pavel ^a  

^a INSTITUTE OF GENE BIOLOGY   (Russian Federation)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; KU ANTIGEN;

ARTICLE; COMPLEX FORMATION; DROSOPHILA; GENE; GENE CONVERSION; GENE FREQUENCY; HET A GENE; KU70 GENE; KU80 GENE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; RETROPOSON; RNA EXTRACTION; TART GENE; TELOMERE;

ANIMALS; ANTIGENS, NUCLEAR; CROSSES, GENETIC; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE CONVERSION; GENE DOSAGE; GENE PRODUCTS, GAG; HETEROZYGOTE; RNA, MESSENGER; TELOMERE; TRANSCRIPTION, GENETIC;

DROSOPHILA MELANOGASTER;

EID: 20444366230     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.034538     Document Type: Article

References (85)

1. ASHBURNER, M., 1989 Drosophila: A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. BAILEY, S. M., J. MEYNE, D. J. CHEN, A. KURIMASA, G. C. LI et al., 1999 DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc. Natl. Acad. Sci. USA 96: 14899-14904.
3. BAUMANN, P., and T. R. CECH, 2000 Protection of telomeres by the Ku protein in fission yeast. Mol. Biol. Cell 11: 3265-3275.
4. BEALL, E. L., and D. C. RIO, 1996 Drosophila IRBP/Ku p70 corresponds to the mutagen-sensitive mus309 gene and is involved in P-element excision in vivo. Genes Dev. 10: 921-933.
5. BEALL, E. L., A. ADMON and D. C. RIO, 1994 A Drosophila protein homologous to the human p70 Ku autoimmune antigen interacts with the P transposable element inverted repeats. Proc. Natl. Acad. Sci. USA 91: 12681-12685.
6. BERTUCH, A. A., and V. LUNDBLAD, 2003a The Ku heterodimer performs separable activities at double-strand breaks and chromosome termini. Mol. Cell. Biol. 23: 8202-8215.
7. BERTUCH, A. A., and V. LUNDBLAD, 2003b Which end: dissecting Ku's function at telomeres and double-strand breaks. Genes Dev. 17: 2347-2350.
8. BI, X., S.-C. D. WEI and Y. S. RONG, 2004 Telomere protection without telomerase: the role of ATM and Mre11 in Drosophila telomere maintenance. Curr. Biol. 14: 1348-1353.
9. BIESSMANN, H., and J. M. MASON, 1988 Progressive loss of DNA sequences from terminal chromosome deficiencies in Drosophila melanogaster. EMBO J. 7: 1081-1086.
10. BIESSMANN, H., S. B. CARTER and J. M. MASON, 1990a Chromosome ends in Drosophila without telomeric DNA sequences. Proc. Natl. Acad. Sci. USA 87: 1758-1761.
11. BIESSMANN, H., J. M. MASON, K. FERRY, M. D'HULST, K. VALGEIRSDOTTIR et al., 1990b Addition of telomere-associated HeT DNA sequences "heals" broken chromosome ends in Drosophila. Cell 61: 663-673.
12. BIESSMANN, H., L. E. CHAMPION, M. O'HAIR, K. IKENAGA, B. KASRAVI et al., 1992a Frequent transpositions of Drosophila melanogaster HeT-A transposable elements to receding chromosome ends. EMBO J. 11: 4459-4469.
13. BIESSMANN, H., K VALGEIRSDOTTIR, A. LOFSKY, C. CHIN, B. GINTHER et al., 1992b HeT-A, a transposable element specifically involved in healing broken chromosome ends in Drosophila melanogaster. Mol. Cell. Biol. 12: 3910-3918.
14. BOULTON, S. J., and S. P. JACKSON, 1996 Identification of a Saccharomyces cerevisiae ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance. Nucleic Acids Res. 24: 4639-4648.
15. BOULTON, S. J., and S. P. JACKSON, 1998 Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17: 1819-1828.
16. BUNDOCK, P., A. H. VAN and P. HOOYKAAS, 2002 Increased telomere length and hypersensitivity to DNA damaging agents in an Arabidopsis KU70 mutant. Nucleic Acids Res. 30: 3395-3400.
17. CASACUBERTA, E., and M. L. PARDUE, 2002 Coevolution of the telomeric retrotransposons across Drosophila species. Genetics 161: 1113-1124.
18. CASACUBERTA, E., and M. L. PARDUE, 2003a HeT-A elements in Drosophila virilis: retrotransposon telomeres are conserved across the Drosophila genus. Proc. Natl. Acad. Sci. USA 100: 14091-14096.
19. CASACUBERTA, E., and M. L. PARDUE, 2003b Transposon telomeres are widely distributed in the Drosophila genus: TART elements in the virilis group. Proc. Natl. Acad. Sci. USA 100: 3363-3368.
20. CENCI, G., G. SIRIACO, G. D. RAFFA, R. KELLUM and M. GATTI, 2003 The Drosophila HOAP protein is required for telomere capping. Nat. Cell Biol. 5: 82-84.
21. CHAI, W. H., L. P. FORD, L. LENERTZ, W. E. WRIGHT and J. W. SHAY, 2002 Human Ku70/80 associates physically with telomerase through interaction with hTERT. J. Biol. Chem. 277: 47242-47247.
22. CHAN, S. W., and E. H. BLACKBURN, 2002 New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 21: 553-563.
23. CIAPPONI, L., G. CENCI, J. DUCAU, C. FLORES, D. M. JOHNSON-SCHLITZ et al., 2004 The Drosophila Mre11/Rad50 complex is required to prevent both telomeric fusion and chromosome breakage. Curr. Biol. 14: 1-20.
24. D'ADDA DI FAGAGNA, F. D., M. P. HANDE, W. M. TONG, D. ROTH, P. M. LANSDORP et al., 2001 Effects of DNA nonhomologous end-joining factors on telomere length and chromosomal stability in mammalian cells. Curr. Biol. 11: 1192-1196.
25. DANILEVSKAYA, O. N., F. SLOT, K. L. TRAVERSE, N. C. HOGAN and M. L. PARDUE, 1994 The Drosophila telomere transposon HeT-A produces a transcript with tightly bound protein. Proc. Natl. Acad. Sci. USA 91: 6679-6682.
26. DANILEVSKAYA, O. N., I. R. ARKHIPOVA, K. L. TRAVERSE and M. L. PARDUE, 1997 Promoting in tandem: the promoter for telomere transposon HeT-A and implications for the evolution of retroviral LTRs. Cell 88: 647-655.
27. DANILEVSKAYA, O. N., K. L. TRAVERSE, N. C. HOGAN, P. G. DEBARYSHE and M. L. PARDUE, 1999 The two Drosophila telomeric transposable elements have very different patterns of transcription. Mol. Cell. Biol. 19: 873-881.
28. DOKE, A. S., A. C. B. DRAKE, S. C. BREWERTON and T. L. BLUNDELL, 2004 Identification of DNA-PK in the arthropods. Evidence for the ancient ancestry of vertebrate non-homologous end-joining. DNA Rep. 3: 33-41.
29. EISSENBERG J. C., T. C. JAMES, D. M. FOSTER-HARTNETT, T. HARTNETT, V. NGAN et al., 1990 Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 87: 9923-9927.
30. ESPEJEL, S., S. FRANCO, S. RODRIGUEZ-PERALES, S. D. BOUFFLER, J. C. CIGUDOSA et al., 2002 Mammalian Ku86 mediates chromosomal fusions and apoptosis caused by critically short telomeres. EMBO J. 21: 2207-2219.
31. FANTI, L., G. GIOVINAZZO, M. BERLOCO and S. PIMPINELLI, 1998 The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol. Cell 2: 527-038.
32. GALLEGO, M. E., N. JALLT and C. I. WHITE, 2003 Telomerase dependence of telomere lengtheningin ku80 mutant Arabidopsis. Plant Cell 15: 782-789.
33. GAUSE, M. H., H. HOVHANNISYAN, T. KAHN, S. KUFITTIG, V. MOGILA et al., 1998 hobo induced rearrangements in the yellow locus influence the insulation effect of the gypsy su(Hw)-binding region of Drosophila melanogaster. Genetics 149: 1393-1405.
34. GEORGE, J. A., and M.-L. PARDUE, 2003 The promoter of the heterochromatin Drosophila telomeric retrotransposon, HeT-A, is active when moved into euchromatic locations. Genetics 163: 625-635.
35. GEYER, P. K., and V. G. CORCES, 1987 Separate regulatory elements are responsible for the complex pattern of tissue-specific and developmental transcription of the fellow locus in Drosophila melanogaster. Genes Dev. 1: 996-1004.
36. GEYER, P. K., C. SPANA and V. G. CORCES, 1986 On the molecular mechanism of gypsy-induced mutations at the yellow locus of Drosophila melanogaster. EMBO J. 5: 2657-2662.
37. GEYER, P. K., M. M. GREEN and V. G. CORCES, 1990 Tissue-specific transcriptional enhancers may act in trans on the gene located in the homologous chromosome: the molecular basis of transvection. EMBO J. 9: 2247-2256.
38. GOLUBOVSKY, M. D., A. Y. KONEV, M. F. WALTER, H. BIESSMANN and J. M. MASON, 2001 Terminal retrotransposons activate a subtelomeric white transgene at the 2L telomere in Drosophila. Genetics 158: 1111-1123.
39. GOYTISOLO, F. A., E. SAMPER, S. EDMONSON, G. E. TACCIOLI and M. A. BLASCO, 2001 The absence of the DNA-dependent protein kinase catalytic subunit in mice results in anaphase bridges and in increased telomeric fusions with normal telomere length and G-strand overhang. Mol. Cell. Biol. 21: 3642-3651.
40. GRAVEL, S., M. LARRIVEE, P. LABRECQUE and R. J. WELLINGER, 1998 Yeast Ku as a regulator of chromosomal DNA end structure. Science 280: 741-744.
41. JACKSON, S. P., 2002 Sensing and repairing DNA double-strand breaks. Carcinogenesis 23: 687-696.
42. JACOBY, D. B., and P. C. WENSINK, 1994 Yolk protein factor 1 is a Drosophila homolog of Ku, the DNA-binding subunit of a DNA-dependent protein kinase from humans. J. Biol. Chem. 269: 11484-11491.
43. JACOBY, D. B., and P. C. WENSINK, 1996 DNA binding specificities of YPF1, a Drosophila homolog to the DNA binding subunit of human DNA-dependent protein kinase. Ku. J. Biol. Chem. 271: 16827-16832.
44. KAHN, T., M. SAVITSKY and P. GEORGIEV, 2000 Attachment of HeT-A sequences to chromosomal termini in Drosophila melanogaster may occur by different mechanisms. Mol. Cell. Biol. 20: 7634-7642.
45. KARESS, R. E., and G. M. RUBIN, 1984 Analysis of P transposable element functions in Drosophila. Cell 38: 135-146.
46. KOIKE, M., 2002 Dimerization, translocation and localization of Ku70 and Ku80 proteins. J. Radiat. Res. 43: 223-236.
47. KUSANO, K., D. M. JOHNSON-SCHLITZ and W. R. ENGELS, 2001 Sterility of Drosophila with mutations in the bloom syndrome gene-complementation by Ku70. Science 291: 2600-2602.
48. LAROCHE, T., S. G. MARTIN, M. GOTTA, H. C. GORHAM, F. E. PRYDE et al., 1998 Mutation of yeast Ku genes disrupts the subnuclear organization of telomeres. Curr. Biol. 8: 653-656.
49. LEVIS, R. W., 1989 Viable deletions of a telomere from a Drosophila chromosome. Cell 58: 791-801.
50. LEVIS, R. W., R. GANESAN, K. HOUTCHENS, L. A. TOLAR and F. M. SHEEN, 1993 Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75: 1083-1093.
51. LINDSLEY, D. L., and G. G. ZIMM. 1992 The Genome of Drosophila melanogaster. Academic Press, San Diego.
52. MARINGELE, L., and D. LYDALL, 2002 EXO1-dependent single-stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70 Delta mutants. Genes Dev. 16: 1919-1933.
53. MARTIN, M., Y. B. MENG and W. CHIA, 1989 Regulatory elements involved in the tissue-specific expression of the yellow gene of Drosophila. Mol. Gen. Genet. 218: 118-126.
54. MASON, J. M., and H. BIESSMANN, 1995 The unusual telomeres of Drosophila. Trends Genet. 11: 58-62.
55. MASON, J. M., E. STROBEL and M. M. GREEN, 1984 mu-2: mutator gene in Drosophila that potentiates the induction of terminal deficiencies. Proc. Natl. Acad. Sci. USA 81: 6090-6094.
56. MASON, J. M., L. E. CHAMPION and C. HOOK, 1997 Germ-line effects of animator, mu2, in Drosophila melanogaster. Genetics 146: 1381-1397.
57. MASON, J. M., A. Y. KONEV, M. D. GOLUBOVSKV and H. BIESSMANN, 2003 Cis- and trans-acting influences on telomeric position effect in Drosophila melanogasler detected with a subterminal transgene. Genetics 163: 917-930.
58. MELNIKOVA, L., and P. GEORGIEV, 2002 Enhancer of terminal gene conversion, a new mutation in Drosophila melanogaster that induces telomere elongation by gene conversion. Genetics 162: 1301-1312.
59. MIKHAILOVSKY, S., T. BELENKAYA and P. GEORGIEV, 1999 Broken chromosomal ends can be elongated by conversion in Drosophila melanogaster. Chrornosoma 108: 114-120.
60. MISHRA, K., and D. SHORE, 1999 Yeast Ku protein plays a direct role in telomeric silencing and counteracts inhibition by Rif proteins. Curr. Biol. 9: 1123-1126.
61. OIKEMUS, S. R., N. MCGINNIS, J. QUEIROZ-MACHADO, H. TUKACHINSKY, S. TAKADA et al., 2004 Drosophila atm/telomere fusion is required for telomeric localization of HP1 and telomere position effect. Genes Dev. 18: 1850-1861.
62. PARDUE, M. L., and P. G. DEBARYSHE, 1999 Drosophila telomeres: two transposable elements with important roles in chromosomes. Genetica 107: 189-196.
63. PARDUE, M. L., and P. G. DEBARYSHE, 2003 Retrotransposons provide an evolutionarily robust non-telomerase mechanism to maintain telomeres. Annu. Rev. Genet. 37: 485-511.
64. PERRINI, B., L. PIACENTINI, L. FANTI, F. ALTIERI, S. CHICHIARELLI et al., 2004 HP1 controls telomere capping, telomere elongation, and telomere silencing by two different mechanisms in Drosophila. Mol. Cell 15: 467-476.
65. PETERSON, S. E., A. E. STELLWAGEN, S. J. DIEDE, M. S. SINGER, Z. W. HAIMBERGER et al., 2001 The function of a stem-loop in telomerase RNA is linked to the DNA repair protein Ku. Nat. Genet. 27: 64-67.
66. POLOTNIANKA, R. M., J. LI and A. J. LUSTIG, 1998 The yeast ku heterodimer is essential for protection of the telomere against nucleolytic and recombinational activities. Curr. Biol. 8: 831-834.
67. PORTER, S. E., P. W. GREENWELL, K. B. RITCHIE and T. D. PETES, 1996 The DNA-binding protein hdf1p (a putative ku homologue) is required for maintaining normal telomere length in Saccharomyces cerevisiae. Nucleic Acids Res. 24: 582-585.
68. QUEIROZ-MACHADO, J., J. PERDIGAO, P. SlMOES-CARVALHO, S. HERRMANN and C. E. SUNKEL, 2001 tef: a mutation that causes telomere fusion and severe genome rearrangements in Drosophila melanogaster. Chromosoma 110: 10-23.
69. RIHA, K., and D. E. SHIPPEN, 2003 Ku is required for telomeric C-rich strand maintenance but not for end-to-end chromosome fusions in Arabidopsis. Proc. Natl. Acad. Sci. USA 100: 611-615.
70. RUBIN, G., and A. C. SPRADLING, 1982 Genetic transformation of Drosophila with transposable element vectors. Science 218: 348-353.
71. RIHA, K., J. M. WATSON, J. PARKEY and D. E. SHIPPEN, 2002 Telomere length deregulation and enhanced sensitivity to genotoxic stress in Arabidopsis mutants deficient in Ku70. EMBO J. 21: 2819-2826.
72. SALDANHA, S. N., L. G. ANDREWS and T. O. TOLLEFSBOL, 2003 Assessment of telomere length and factors that contribute to its stability. Eur. J. Biochem. 270: 389-403.
73. SAMBROOK, J., E. F. FRITSCH and T. MANIATIS, 1989 Molecular Cloning: A. Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
74. SAMPER, E., F. A. GOYTISOLO, P. SLIJEPCEVIC, P. P. W. VANBUUL and M. A. BLASCO, 2000 Mammalian Ku86 protein prevents telomeric fusions independently of the length of TTAGGG repeats and the G-strand overhang. EMBO Rep. 1: 244-252.
75. SAVITSKY, M., O. KRAVCHUK, L. MELNIKOVA and P. GEORGIEV, 2002 Heterochromatin protein 1 is involved in control of telomere elongation in Drosophila melanogaster. Mol. Cell. Biol. 22: 3204-3218.
76. SHAREEF, M. M., C. KING, M. DAMAJ, R. BADAGU, D. W. HUANG et al., 2001 Drosophila heterochromatin protein 1 (HPI)/origin recognition complex (ORC) protein is associated with HP1 and ORC and functions in heterochromatin-induced silencing. Mol. Biol. Cell 12: 1671-1685.
77. SHEEN, F. M., and R. W. LEVIS, 1994 Transposition of the LINE-like retrotransposon TART to Drosophila chromosome termini. Proc. Natl. Acad. Sci. USA 91: 12510-12514.
78. SILVA, E., S. TIONG, M. PEDERSEN, E. HOMOLA, E. ROYOU et al., 2004 ATM is required for telomere maintenance and chromosome stability during Drosophila development. Curr. Biol. 14: 1341-1347.
79. SIRIACO, G. M., G. CENCI, A. HAOUDI, L. E. CHAMPION, C. ZHOU et al., 2002 Telomere elongation (Tel), a new mutation in Drosophila melanogaster that produces long telomeres. Genetics 160: 235-245.
80. SMITH, G. C. M., and S. P. JACKSON, 1999 The DNA-dependent protein kinase. Gene Dev. 13: 916-934.
81. STELLWAGEN, A. E., Z. W. HAIMBERGER, J. R. VEATCH and D. E. GOTTSCHLING, 2003 Ku interacts with telomerase RNA to promote telomere addition at native and broken chromosome ends. Genes Dev. 17: 2384-2395.
82. VAX STEENSEL, B., A. SMOGORZEWSKA and T. DE LANGE, 1998 TRF2 protects human telomeres from end-to-end fusions. Cell 92: 401-413.
83. WALKER, J. R., R. A. CORPINA and J. GOLDBERG, 2001 Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 412: 607-614.
84. WALTER, M. F., B. C. BEACK, G. AFSHAR, A.-Y. KERMABON, T. R. F. WRIGHT et al., 1991 Temporal and spatial expression of the yellow gene in correlation with cuticle formation and DOPA decarboxylase activity in Drosophila development. Dev. Biol. 147: 32-45.
85. WEI, C., and M. PRICE, 2003 Protecting the terminus: t-loops and telomere end-binding proteins. Cell. Mol. Life Sci. 60:2283-2294.