RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase

Genetics

Volumn 152, Issue 1, 1999, Pages 143-152

  Le, Siyuan ^a,b   Moore, J Kent ^c,d   Haber, James E ^c   Greider, Carol W ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^c BRANDEIS UNIVERSITY   (United States)

^d Exact Sciences Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TELOMERASE;

ARTICLE; CELL DEATH; CELL VIABILITY; CHROMOSOME SIZE; ENZYME ACTIVITY; EPISTASIS; GENE CONVERSION; GENE DELETION; GENE MUTATION; GENETIC RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; TELOMERE; YEAST;

BLOTTING, SOUTHERN; CELL DIVISION; CELL SURVIVAL; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; EPISTASIS, GENETIC; EXODEOXYRIBONUCLEASES; FUNGAL PROTEINS; GENOTYPE; MUTAGENESIS; RAD51 RECOMBINASE; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINATION, GENETIC; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERASE; TELOMERE; TIME FACTORS;

EID: 0032959506     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (74)

1. ALANI, E., R. PADMORE and N. KLECKNER, 1990 Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61: 419-436.
2. AUTEXIER, C., and C. W. GREIDER, 1996 Telomerase and cancer: revisiting the telomere hypothesis. Trends Biochem. Sci. 21: 387-391.
3. BAI, Y., and L. S. SYMINGTON, 1996 A Rad52 homolog is required for RAD51-independent mitotic recombination in Saccharomyces cerevisiae. Genes Dev. 10: 2025-2037.
4. BERNARDS, A., P. A. M. MICHELS, C. R. LINCKE and P. BORST, 1983 Growth of chromosomal ends in multiplying trypanosomes. Nature 303: 592-597.
5. BLACKBURN, E. H., and J. W. SZOSTAK, 1984 The molecular structure of centromeres and telomeres. Annu. Rev. Biochem. 53: 163-194.
6. BLASCO, M. A., H.-W. LEE, P. M. HANDE, E. SAMPER, P. M. LANSDORP et al., 1997 Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91: 25-34.
7. BOSCO, G., and J. E. HABER, 1998 Chromosome break-induced DNA replication leads to non-reciprocal translocations and telomere capture. Genetics 150: 1037-1047.
8. 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.
9. 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.
10. BRYAN, T. M., A. ENGLEZOU, J. GUPTA, S. BACCHETTI and R. R. REDDEL, 1995 Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J. 14: 4240-4248.
11. BRYAN, T. M., A. ENGLEZOU, L. DALLA-POZZA, M. A. DUNHAM and R. R. REDDEL, 1997 Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med. 3: 1271-1274.
12. CLEVER, B., H. INTERTHAL, J. SCHMUCKLI-MAURER, J. KING, M. SIGRIST et al., 1997 Recombinational repair in yeast: functional interactions between Rad51 and Rad54 proteins. EMBO J. 16: 2535-2544.
13. DONOVAN, J. W., G. T. MILNE and D. T. WEAVER, 1994 Homotypic and heterotypic protein associations control Rad51 function in double-strand break repair. Genes Dev. 8: 2552-2562.
14. DUNN, B., P. SZAUTER, M. L. PARDUE and J. W. SZOSTAK, 1985 Transfer of yeast telomeres to linear plasmids by recombination. Cell 39: 191-201.
15. FRIEDBERG, E. C., 1988 Deoxyribonucleic acid repair in the yeast Saccharomyces cerevisiae. Microbiol. Rev. 52: 70-102.
16. FURUSE, M., Y. NAGASE, H. TSUBOUCHI, K. MURAKAMI-MUROFUSHI, T. SHIBATA et al., 1998 Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J. 17: 6412-6425.
17. 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.
18. GREIDER, C. W., 1996 Telomere length regulation. Annu. Rev. Biochem. 65: 337-365.
19. HABER, J. E., 1995 In vivo biochemistry: physical monitoring of recombination induced by site-specific endonucleases. Bioessays 17: 609-620.
20. HABER, J. E., 1998 The many interfaces of Mre11. Cell 95: 583-586.
21. HAYS, S. L., A. A. FIRMENICH and P. BERG, 1995 Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins. Proc. Natl. Acad. Sci. USA 92: 6925-6929.
22. HOROWITZ, H., and J. E. HABER, 1984 Subtelomeric regions of yeast chromosomes contain a 36 base pair tandemly repeated sequence. Nucleic Acids Res. 12: 7105-7121.
23. IVANOV, E. L., and J. E. HABER, 1997 DNA repair: RAD alert. Curr. Biol. 7: R492-495.
24. IVANOV, E. L., N. SUGAWARA, C. I. WHITE, F. FABRE and J. E. HABER, 1994 Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 14: 3414-3425.
25. IVANOV, E. L., N. SUGAWARA, J. FISHMAN-LOBELL and J. E. HABER, 1996 Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics 142: 693-704.
26. JIANG, H., Y. XIE, P. HOUSTON, K. STEMKE-HALE, U. H. MORTENSEN et al., 1996 Direct association between the yeast Rad51 and Rad54 recombination proteins. J. Biol. Chem. 271: 33181-33186.
27. JOHZUKA, K., and H. OGAWA, 1995 Interaction of Mre11 and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics 139: 1521-1532.
28. KANAAR, R., and J. H. J. HOEIJMAKERS, 1997 Recombination and joining: Different means to the same ends. Genes Function 1: 165-174.
29. KIRONMAI, K. M., and K. MUNIYAPPA, 1997 Alteration of telomeric sequences and senescence caused by mutations in RAD50 of Saccharomyces cerevisiae. Genes Cells 2: 443-455.
30. KRAMER, K. M., J. A. BROCK, K. BLOOM, J. K. MOORE and J. E. HABER, 1994 Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events. Mol. Cell. Biol. 14: 1293-1301.
31. LENDVAY, T. S., D. K. MORRIS, J. SAH, B. BALASUBRAMANIAN and V. LUNDBLAD, 1996 Senescence mutants of Saccharomyces cerevisiae with a defect in telomere replication identify three additional EST genes. Genetics 144: 1399-1412.
32. LINGNER, J., T. R. HUGHES, A. SHEVCHENKO, M. MANN, V. LUNDBLAD et al., 1997 Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276: 561-567.
33. LOUIS, E., and J. E. HABER, 1990a Mitotic recombination among subtelomeric Y′ repeats in Saccharomyres cerevisiae. Genetics 124: 547-559.
34. LOUIS, E. J., and J. E. HABER, 1990b The subtelomeric y′ repeat family in Saccharomyces cerevisiae an experimental system for repeated sequence evolution. Genetics 124: 533-545.
35. LUNDBLAD, V., and E. H. BLACKBURN, 1993 An alternative pathway for yeast telomere maintenance rescues est1-senescence. Cell 73: 347-360.
36. MALKOVA, A., E. L. IVANOV and J. E. HABER, 1996a Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc. Natl. Acad. Sci. USA 93: 7131-7136.
37. MALKOVA, A., L. ROSS, D. DAWSON, M. F. HOEKSTRA and J. E. HABER, 1996b Meiotic recombination initiated by a double-strand break in rad50 delta yeast cells otherwise unable to initiate meiotic recombination. Genetics 143: 741-754.
38. MALONE, R. E., T. WARD, S. LIN and J. WARING, 1990 The RAD50 gene, a member of the double strand break repair epistasis group, is not required for spontaneous mitotic recombination in yeast. Curr. Genet. 18: 111-116.
39. MCDONALD, J. P., and R. ROTHSTEIN, 1994 Unrepaired heteroduplex DNA in Saccharomyces cerevisiae is decreased in RAD1 RAD52-independent recombination. Genetics 137: 393-405.
40. MILNE, G. T., S. JIN, K. B. SHANNON and D. T. WEAVER, 1996 Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 4189-4198.
41. MOORE, J. K., and J. E. HABER, 1996 Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 2164-2173.
42. MOREAU, S., H. R. FERGUSON and L. S. SYMINGTON, 1999 The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining or telomere maintenance. Mol. Cell. Biol. 19: 556-566.
43. MORROW, D. M., C. CONNELLY and P. HIETER, 1997 "Break copy" duplication: a model for chromosome fragment formation in Saccharomyces cerevisiae. Genetics 147: 371-382.
44. MORTIMER, R. K., R. CONTOPOULOU and D. SCHILD, 1981 Mitotic chromosome loss in a radiation-sensitive strain of the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 78: 5778-5782.
45. NUGENT, C. I., and V. LUNDBLAD, 1998 The telomerase reverse transcriptase: components and regulation. Genes Dev. 12: 1073-1085.
46. NUGENT, C. I., G. BOSCO, L. O. ROSS, S. K. EVANS, A. P. SALINGER et al., 1998 Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr. Biol. 8: 657-660.
47. OGAWA, H., K. JOHZUKA, T. NAKAGAWA, S. H. LEEM and A. H. HAGIHARA, 1995 Functions of the yeast meiotic recombination genes, MRE11 and MRE2. Adv. Biophys. 31: 67-76.
48. PETES, T. D., R. E. MALONE and L. S. SYMINGTON, 1991 Recombination in yeast, pp. 407-522 in The Molecular and Cellular Biology of the Yeast Saccharomyces, edited byJ. R. BROACH, J. R. PRINGLE and E. W. JONES. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
49. PLUTA, A. F., and V. A. ZAKIAN, 1989 Recombination occurs during telomere formation in yeast. Nature 337: 429-433.
50. 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.
51. PORTER, S. E., P. W. GREENWELL, K. B. RITCHIE and T. D. PETES, 1996 The DNA-binding protein Hdflp (a putative Ku homologue) is required for maintaining normal telomere length in Saccharomyces cerevisiae. Nucleic Acids Res. 24: 582-585.
52. PRESCOTT, J., and E. H. BLACKBURN, 1997 Telomerase RNA mutations in Saccharomyces cerevisiae alter telomerase action and reveal nonprocessivity in vivo and in vitro. Genes Dev. 11: 528-540.
53. RATTRAY, A. J., and L. S. SYMINGTON, 1994 Use of a chromosomal inverted repeat to demonstrate that the RAD51 and RAD52 genes of Saccharomyces cerevisiae have different roles in mitotic recombination. Genetics 138: 587-595.
54. RATTRAY, A. J., and L. S. SYMINGTON, 1995 Multiple pathways for homologous recombination in Saccharomyces cerevisiae. Genetics 139: 45-56.
55. REDDEL, R. R., T. M. BRYAN and J. P. MURNANE, 1997 Immortalized cells with no detectable telomerase activity: a review. Biochemistry 62: 1254-1262.
56. ROSE, M. D., F. WINSTON and P. HEITER, 1988 Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
57. RUDIN, N., E. SUGARMAN and J. E. HABER, 1989 Genetic and physical analysis of double-strand break repair and recombination in Saccharomyces cerevisiae. Genetics 122: 519-534.
58. SANDELL, L. L., and V. A. ZAKIAN, 1993 Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell 75: 729-739.
59. SHAMPAY, J., and E. H. BLACKBURN, 1988 Generation of telomere-length heterogeneity in Saccharomyces cerevisiae. Proc. Nat. Acad. Sci. USA 85: 534-538.
60. SHARPLES, G. J., and D. R. LEACH, 1995 Structural and functional similarities between the SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) recombination and repair proteins of yeast [letter]. Mol. Microbiol. 17: 1215-1217.
61. SHINOHARA, A., H. OGAWA and T. OGAWA, 1992 Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein [published erratum appears in Cell 1992 Oct 2;71(1):following 180]. Cell 69: 457-470.
62. SINGER, M. S., and D. E. GOTTSCHLING, 1994 TLC1: Template RNA component of Saccharomyces cerevisiae telomerase. Science 266: 404-409.
63. SUGAWARA, N., and J. E. HABER, 1992 Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation. Mol. Cell. Biol. 12: 563-575.
64. SUGAWARA, N., E. L. IVANOV, J. FISHMAN-LOBELL, B. L. RAY, X. WU et al., 1995 DNA structure-dependent requirements for yeast RAD genes in gene conversion. Nature 373: 84-86.
65. SUNG, P., 1997 Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. Genes Dev. 11: 1111-1121.
66. SZOSTAK, J. W., T. L. ORR-WEAVER, R. J. ROTHSTEIN and F. W. STAHL, 1983 The double-strand-break repair model for recombination. Cell 33: 25-35.
67. TSUBOUCHI, H., and H. OGAWA, 1998 A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol. Cell. Biol. 18: 260-268.
68. TSUKAMOTO, Y., and H. IKEDA, 1998 Double-strand break repair mediated by DNA end-joining. Genes Cells 3: 135-144.
69. TSUKAMOTO, Y., J. KATO and H. IKEDA, 1996 Hdf1, a yeast Ku-protein homologue, is involved in illegitimate recombination, but not in homologous recombination. Nucleic Acids Res. 24: 2067-2072.
70. TSUKAMOTO, Y., J. KATO and H. IKEDA, 1997 Silencing factors participate in DNA repair and recombination in Saccharomyces cerevisiae [see comments]. Nature 388: 900-903.
71. USUI, T., T. OHTA, H. OSHUMI, H. TSUBOUCHI, J.-I. TOMIZAWA et al., 1998 Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell 95: 706-716.
72. WALMSLEY, R. W., C. S. M. CHAN, B.-K. TYE and T. D. PETES, 1984 Unusual DNA sequences associated with the ends of yeast chromosomes. Nature 310: 157-160.
73. ZAKIAN, V. A., 1989 Structure and function of telomeres. Annu. Rev. Genet. 23: 579-604.
74. ZAKIAN, V. A., 1996 Structure, function, and replication of Saccharomyces cerevisiae telomeres. Annu. Rev. Genet. 30: 141-172.