Skip to main content
Genetics logoLink to Genetics
. 2002 Aug;161(4):1437–1452. doi: 10.1093/genetics/161.4.1437

Telomere binding of checkpoint sensor and DNA repair proteins contributes to maintenance of functional fission yeast telomeres.

Toru M Nakamura 1, Bettina A Moser 1, Paul Russell 1
PMCID: PMC1462227  PMID: 12196391

Abstract

Telomeres, the ends of linear chromosomes, are DNA double-strand ends that do not trigger a cell cycle arrest and yet require checkpoint and DNA repair proteins for maintenance. Genetic and biochemical studies in the fission yeast Schizosaccharomyces pombe were undertaken to understand how checkpoint and DNA repair proteins contribute to telomere maintenance. On the basis of telomere lengths of mutant combinations of various checkpoint-related proteins (Rad1, Rad3, Rad9, Rad17, Rad26, Hus1, Crb2, Chk1, Cds1), Tel1, a telomere-binding protein (Taz1), and DNA repair proteins (Ku70, Rad32), we conclude that Rad3/Rad26 and Tel1/Rad32 represent two pathways required to maintain telomeres and prevent chromosome circularization. Rad1/Rad9/Hus1/Rad17 and Ku70 are two additional epistasis groups, which act in the Rad3/Rad26 pathway. However, Rad3/Rad26 must have additional target(s), as cells lacking Tel1/Rad32, Rad1/Rad9/Hus1/Rad17, and Ku70 groups did not circularize chromosomes. Cells lacking Rad3/Rad26 and Tel1/Rad32 senesced faster than a telomerase trt1Delta mutant, suggesting that these pathways may contribute to telomere protection. Deletion of taz1 did not suppress chromosome circularization in cells lacking Rad3/Rad26 and Tel1/Rad32, also suggesting that two pathways protect telomeres. Chromatin immunoprecipitation analyses found that Rad3, Rad1, Rad9, Hus1, Rad17, Rad32, and Ku70 associate with telomeres. Thus, checkpoint sensor and DNA repair proteins contribute to telomere maintenance and protection through their association with telomeres.

Full Text

The Full Text of this article is available as a PDF (443.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ahmed S., Hodgkin J. MRT-2 checkpoint protein is required for germline immortality and telomere replication in C. elegans. Nature. 2000 Jan 13;403(6766):159–164. doi: 10.1038/35003120. [DOI] [PubMed] [Google Scholar]
  2. Bao S., Tibbetts R. S., Brumbaugh K. M., Fang Y., Richardson D. A., Ali A., Chen S. M., Abraham R. T., Wang X. F. ATR/ATM-mediated phosphorylation of human Rad17 is required for genotoxic stress responses. Nature. 2001 Jun 21;411(6840):969–974. doi: 10.1038/35082110. [DOI] [PubMed] [Google Scholar]
  3. Baumann P., Cech T. R. Pot1, the putative telomere end-binding protein in fission yeast and humans. Science. 2001 May 11;292(5519):1171–1175. doi: 10.1126/science.1060036. [DOI] [PubMed] [Google Scholar]
  4. Baumann P., Cech T. R. Protection of telomeres by the Ku protein in fission yeast. Mol Biol Cell. 2000 Oct;11(10):3265–3275. doi: 10.1091/mbc.11.10.3265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bentley N. J., Holtzman D. A., Flaggs G., Keegan K. S., DeMaggio A., Ford J. C., Hoekstra M., Carr A. M. The Schizosaccharomyces pombe rad3 checkpoint gene. EMBO J. 1996 Dec 2;15(23):6641–6651. [PMC free article] [PubMed] [Google Scholar]
  6. Blackburn E. H. Switching and signaling at the telomere. Cell. 2001 Sep 21;106(6):661–673. doi: 10.1016/s0092-8674(01)00492-5. [DOI] [PubMed] [Google Scholar]
  7. Boddy M. N., Furnari B., Mondesert O., Russell P. Replication checkpoint enforced by kinases Cds1 and Chk1. Science. 1998 May 8;280(5365):909–912. doi: 10.1126/science.280.5365.909. [DOI] [PubMed] [Google Scholar]
  8. Boulton S. J., Jackson S. P. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 1998 Mar 16;17(6):1819–1828. doi: 10.1093/emboj/17.6.1819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brush G. S., Kelly T. J. Phosphorylation of the replication protein A large subunit in the Saccharomyces cerevisiae checkpoint response. Nucleic Acids Res. 2000 Oct 1;28(19):3725–3732. doi: 10.1093/nar/28.19.3725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bähler J., Wu J. Q., Longtine M. S., Shah N. G., McKenzie A., 3rd, Steever A. B., Wach A., Philippsen P., Pringle J. R. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast. 1998 Jul;14(10):943–951. doi: 10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y. [DOI] [PubMed] [Google Scholar]
  11. Cai R. L., Yan-Neale Y., Cueto M. A., Xu H., Cohen D. HDAC1, a histone deacetylase, forms a complex with Hus1 and Rad9, two G2/M checkpoint Rad proteins. J Biol Chem. 2000 Sep 8;275(36):27909–27916. doi: 10.1074/jbc.M000168200. [DOI] [PubMed] [Google Scholar]
  12. Caspari T., Carr A. M. DNA structure checkpoint pathways in Schizosaccharomyces pombe. Biochimie. 1999 Jan-Feb;81(1-2):173–181. doi: 10.1016/s0300-9084(99)80050-9. [DOI] [PubMed] [Google Scholar]
  13. Caspari T., Dahlen M., Kanter-Smoler G., Lindsay H. D., Hofmann K., Papadimitriou K., Sunnerhagen P., Carr A. M. Characterization of Schizosaccharomyces pombe Hus1: a PCNA-related protein that associates with Rad1 and Rad9. Mol Cell Biol. 2000 Feb;20(4):1254–1262. doi: 10.1128/mcb.20.4.1254-1262.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chan S. W., Chang J., Prescott J., Blackburn E. H. Altering telomere structure allows telomerase to act in yeast lacking ATM kinases. Curr Biol. 2001 Aug 21;11(16):1240–1250. doi: 10.1016/s0960-9822(01)00391-8. [DOI] [PubMed] [Google Scholar]
  15. Cooper J. P., Nimmo E. R., Allshire R. C., Cech T. R. Regulation of telomere length and function by a Myb-domain protein in fission yeast. Nature. 1997 Feb 20;385(6618):744–747. doi: 10.1038/385744a0. [DOI] [PubMed] [Google Scholar]
  16. Corda Y., Schramke V., Longhese M. P., Smokvina T., Paciotti V., Brevet V., Gilson E., Géli V. Interaction between Set1p and checkpoint protein Mec3p in DNA repair and telomere functions. Nat Genet. 1999 Feb;21(2):204–208. doi: 10.1038/5991. [DOI] [PubMed] [Google Scholar]
  17. Dahlen M., Olsson T., Kanter-Smoler G., Ramne A., Sunnerhagen P. Regulation of telomere length by checkpoint genes in Schizosaccharomyces pombe. Mol Biol Cell. 1998 Mar;9(3):611–621. doi: 10.1091/mbc.9.3.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Diede S. J., Gottschling D. E. Exonuclease activity is required for sequence addition and Cdc13p loading at a de novo telomere. Curr Biol. 2001 Sep 4;11(17):1336–1340. doi: 10.1016/s0960-9822(01)00400-6. [DOI] [PubMed] [Google Scholar]
  19. Edwards R. J., Bentley N. J., Carr A. M. A Rad3-Rad26 complex responds to DNA damage independently of other checkpoint proteins. Nat Cell Biol. 1999 Nov;1(7):393–398. doi: 10.1038/15623. [DOI] [PubMed] [Google Scholar]
  20. Ferreira M. G., Cooper J. P. The fission yeast Taz1 protein protects chromosomes from Ku-dependent end-to-end fusions. Mol Cell. 2001 Jan;7(1):55–63. doi: 10.1016/s1097-2765(01)00154-x. [DOI] [PubMed] [Google Scholar]
  21. Gatei M., Young D., Cerosaletti K. M., Desai-Mehta A., Spring K., Kozlov S., Lavin M. F., Gatti R. A., Concannon P., Khanna K. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat Genet. 2000 May;25(1):115–119. doi: 10.1038/75508. [DOI] [PubMed] [Google Scholar]
  22. Goedecke W., Eijpe M., Offenberg H. H., van Aalderen M., Heyting C. Mre11 and Ku70 interact in somatic cells, but are differentially expressed in early meiosis. Nat Genet. 1999 Oct;23(2):194–198. doi: 10.1038/13821. [DOI] [PubMed] [Google Scholar]
  23. Grandin N., Damon C., Charbonneau M. Cdc13 prevents telomere uncapping and Rad50-dependent homologous recombination. EMBO J. 2001 Nov 1;20(21):6127–6139. doi: 10.1093/emboj/20.21.6127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gravel S., Larrivée M., Labrecque P., Wellinger R. J. Yeast Ku as a regulator of chromosomal DNA end structure. Science. 1998 May 1;280(5364):741–744. doi: 10.1126/science.280.5364.741. [DOI] [PubMed] [Google Scholar]
  25. Griffith Jack D., Lindsey-Boltz Laura A., Sancar Aziz. Structures of the human Rad17-replication factor C and checkpoint Rad 9-1-1 complexes visualized by glycerol spray/low voltage microscopy. J Biol Chem. 2002 Mar 20;277(18):15233–15236. doi: 10.1074/jbc.C200129200. [DOI] [PubMed] [Google Scholar]
  26. Griffiths D. J., Barbet N. C., McCready S., Lehmann A. R., Carr A. M. Fission yeast rad17: a homologue of budding yeast RAD24 that shares regions of sequence similarity with DNA polymerase accessory proteins. EMBO J. 1995 Dec 1;14(23):5812–5823. doi: 10.1002/j.1460-2075.1995.tb00269.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Grimm C., Kohli J., Murray J., Maundrell K. Genetic engineering of Schizosaccharomyces pombe: a system for gene disruption and replacement using the ura4 gene as a selectable marker. Mol Gen Genet. 1988 Dec;215(1):81–86. doi: 10.1007/BF00331307. [DOI] [PubMed] [Google Scholar]
  28. Hardy C. F., Sussel L., Shore D. A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation. Genes Dev. 1992 May;6(5):801–814. doi: 10.1101/gad.6.5.801. [DOI] [PubMed] [Google Scholar]
  29. Hartsuiker E., Vaessen E., Carr A. M., Kohli J. Fission yeast Rad50 stimulates sister chromatid recombination and links cohesion with repair. EMBO J. 2001 Dec 3;20(23):6660–6671. doi: 10.1093/emboj/20.23.6660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hsu H. L., Gilley D., Blackburn E. H., Chen D. J. Ku is associated with the telomere in mammals. Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12454–12458. doi: 10.1073/pnas.96.22.12454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hsu H. L., Gilley D., Galande S. A., Hande M. P., Allen B., Kim S. H., Li G. C., Campisi J., Kohwi-Shigematsu T., Chen D. J. Ku acts in a unique way at the mammalian telomere to prevent end joining. Genes Dev. 2000 Nov 15;14(22):2807–2812. doi: 10.1101/gad.844000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kai M., Tanaka H., Wang T. S. Fission yeast Rad17 associates with chromatin in response to aberrant genomic structures. Mol Cell Biol. 2001 May;21(10):3289–3301. doi: 10.1128/MCB.21.10.3289-3301.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kanoh J., Ishikawa F. spRap1 and spRif1, recruited to telomeres by Taz1, are essential for telomere function in fission yeast. Curr Biol. 2001 Oct 16;11(20):1624–1630. doi: 10.1016/s0960-9822(01)00503-6. [DOI] [PubMed] [Google Scholar]
  34. Kaur R., Kostrub C. F., Enoch T. Structure-function analysis of fission yeast Hus1-Rad1-Rad9 checkpoint complex. Mol Biol Cell. 2001 Dec;12(12):3744–3758. doi: 10.1091/mbc.12.12.3744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Khanna K. K., Jackson S. P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet. 2001 Mar;27(3):247–254. doi: 10.1038/85798. [DOI] [PubMed] [Google Scholar]
  36. Kishi S., Zhou X. Z., Ziv Y., Khoo C., Hill D. E., Shiloh Y., Lu K. P. Telomeric protein Pin2/TRF1 as an important ATM target in response to double strand DNA breaks. J Biol Chem. 2001 May 25;276(31):29282–29291. doi: 10.1074/jbc.M011534200. [DOI] [PubMed] [Google Scholar]
  37. Kondo T., Wakayama T., Naiki T., Matsumoto K., Sugimoto K. Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science. 2001 Oct 26;294(5543):867–870. doi: 10.1126/science.1063827. [DOI] [PubMed] [Google Scholar]
  38. Kostrub C. F., al-Khodairy F., Ghazizadeh H., Carr A. M., Enoch T. Molecular analysis of hus1+, a fission yeast gene required for S-M and DNA damage checkpoints. Mol Gen Genet. 1997 Apr 28;254(4):389–399. doi: 10.1007/pl00008606. [DOI] [PubMed] [Google Scholar]
  39. Krawchuk M. D., Wahls W. P. High-efficiency gene targeting in Schizosaccharomyces pombe using a modular, PCR-based approach with long tracts of flanking homology. Yeast. 1999 Sep 30;15(13):1419–1427. doi: 10.1002/(SICI)1097-0061(19990930)15:13<1419::AID-YEA466>3.0.CO;2-Q. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lieberman H. B., Hopkins K. M., Laverty M., Chu H. M. Molecular cloning and analysis of Schizosaccharomyces pombe rad9, a gene involved in DNA repair and mutagenesis. Mol Gen Genet. 1992 Apr;232(3):367–376. doi: 10.1007/BF00266239. [DOI] [PubMed] [Google Scholar]
  41. Lim D. S., Kim S. T., Xu B., Maser R. S., Lin J., Petrini J. H., Kastan M. B. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature. 2000 Apr 6;404(6778):613–617. doi: 10.1038/35007091. [DOI] [PubMed] [Google Scholar]
  42. Lombard D. B., Guarente L. Nijmegen breakage syndrome disease protein and MRE11 at PML nuclear bodies and meiotic telomeres. Cancer Res. 2000 May 1;60(9):2331–2334. [PubMed] [Google Scholar]
  43. Longhese M. P., Paciotti V., Neecke H., Lucchini G. Checkpoint proteins influence telomeric silencing and length maintenance in budding yeast. Genetics. 2000 Aug;155(4):1577–1591. doi: 10.1093/genetics/155.4.1577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Manolis K. G., Nimmo E. R., Hartsuiker E., Carr A. M., Jeggo P. A., Allshire R. C. Novel functional requirements for non-homologous DNA end joining in Schizosaccharomyces pombe. EMBO J. 2001 Jan 15;20(1-2):210–221. doi: 10.1093/emboj/20.1.210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Matsuura A., Naito T., Ishikawa F. Genetic control of telomere integrity in Schizosaccharomyces pombe: rad3(+) and tel1(+) are parts of two regulatory networks independent of the downstream protein kinases chk1(+) and cds1(+). Genetics. 1999 Aug;152(4):1501–1512. doi: 10.1093/genetics/152.4.1501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Melo J. A., Cohen J., Toczyski D. P. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 2001 Nov 1;15(21):2809–2821. doi: 10.1101/gad.903501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Moser B. A., Brondello J. M., Baber-Furnari B., Russell P. Mechanism of caffeine-induced checkpoint override in fission yeast. Mol Cell Biol. 2000 Jun;20(12):4288–4294. doi: 10.1128/mcb.20.12.4288-4294.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Murray J. M., Carr A. M., Lehmann A. R., Watts F. Z. Cloning and characterisation of the rad9 DNA repair gene from Schizosaccharomyces pombe. Nucleic Acids Res. 1991 Jul 11;19(13):3525–3531. doi: 10.1093/nar/19.13.3525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Naito T., Matsuura A., Ishikawa F. Circular chromosome formation in a fission yeast mutant defective in two ATM homologues. Nat Genet. 1998 Oct;20(2):203–206. doi: 10.1038/2517. [DOI] [PubMed] [Google Scholar]
  50. Nakamura T. M., Morin G. B., Chapman K. B., Weinrich S. L., Andrews W. H., Lingner J., Harley C. B., Cech T. R. Telomerase catalytic subunit homologs from fission yeast and human. Science. 1997 Aug 15;277(5328):955–959. doi: 10.1126/science.277.5328.955. [DOI] [PubMed] [Google Scholar]
  51. Nugent C. I., Bosco G., Ross L. O., Evans S. K., Salinger A. P., Moore J. K., Haber J. E., Lundblad V. Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr Biol. 1998 May 21;8(11):657–660. doi: 10.1016/s0960-9822(98)70253-2. [DOI] [PubMed] [Google Scholar]
  52. Oakley G. G., Loberg L. I., Yao J., Risinger M. A., Yunker R. L., Zernik-Kobak M., Khanna K. K., Lavin M. F., Carty M. P., Dixon K. UV-induced hyperphosphorylation of replication protein a depends on DNA replication and expression of ATM protein. Mol Biol Cell. 2001 May;12(5):1199–1213. doi: 10.1091/mbc.12.5.1199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Orlando V., Paro R. Mapping Polycomb-repressed domains in the bithorax complex using in vivo formaldehyde cross-linked chromatin. Cell. 1993 Dec 17;75(6):1187–1198. doi: 10.1016/0092-8674(93)90328-n. [DOI] [PubMed] [Google Scholar]
  54. Paciotti V., Lucchini G., Plevani P., Longhese M. P. Mec1p is essential for phosphorylation of the yeast DNA damage checkpoint protein Ddc1p, which physically interacts with Mec3p. EMBO J. 1998 Jul 15;17(14):4199–4209. doi: 10.1093/emboj/17.14.4199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Post S., Weng Y. C., Cimprich K., Chen L. B., Xu Y., Lee E. Y. Phosphorylation of serines 635 and 645 of human Rad17 is cell cycle regulated and is required for G(1)/S checkpoint activation in response to DNA damage. Proc Natl Acad Sci U S A. 2001 Oct 30;98(23):13102–13107. doi: 10.1073/pnas.231364598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Rigaut G., Shevchenko A., Rutz B., Wilm M., Mann M., Séraphin B. A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol. 1999 Oct;17(10):1030–1032. doi: 10.1038/13732. [DOI] [PubMed] [Google Scholar]
  57. Ritchie K. B., Mallory J. C., Petes T. D. 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. 1999 Sep;19(9):6065–6075. doi: 10.1128/mcb.19.9.6065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Ritchie K. B., Petes T. D. The Mre11p/Rad50p/Xrs2p complex and the Tel1p function in a single pathway for telomere maintenance in yeast. Genetics. 2000 May;155(1):475–479. doi: 10.1093/genetics/155.1.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Saka Y., Esashi F., Matsusaka T., Mochida S., Yanagida M. Damage and replication checkpoint control in fission yeast is ensured by interactions of Crb2, a protein with BRCT motif, with Cut5 and Chk1. Genes Dev. 1997 Dec 15;11(24):3387–3400. doi: 10.1101/gad.11.24.3387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Strahl-Bolsinger S., Hecht A., Luo K., Grunstein M. SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes Dev. 1997 Jan 1;11(1):83–93. doi: 10.1101/gad.11.1.83. [DOI] [PubMed] [Google Scholar]
  61. Sunnerhagen P., Seaton B. L., Nasim A., Subramani S. Cloning and analysis of a gene involved in DNA repair and recombination, the rad1 gene of Schizosaccharomyces pombe. Mol Cell Biol. 1990 Jul;10(7):3750–3760. doi: 10.1128/mcb.10.7.3750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Tavassoli M., Shayeghi M., Nasim A., Watts F. Z. Cloning and characterisation of the Schizosaccharomyces pombe rad32 gene: a gene required for repair of double strand breaks and recombination. Nucleic Acids Res. 1995 Feb 11;23(3):383–388. doi: 10.1093/nar/23.3.383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Tsukamoto Y., Taggart A. K., Zakian V. A. The role of the Mre11-Rad50-Xrs2 complex in telomerase- mediated lengthening of Saccharomyces cerevisiae telomeres. Curr Biol. 2001 Sep 4;11(17):1328–1335. doi: 10.1016/s0960-9822(01)00372-4. [DOI] [PubMed] [Google Scholar]
  64. Usui T., Ogawa H., Petrini J. H. A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol Cell. 2001 Jun;7(6):1255–1266. doi: 10.1016/s1097-2765(01)00270-2. [DOI] [PubMed] [Google Scholar]
  65. Venclovas C., Thelen M. P. Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes. Nucleic Acids Res. 2000 Jul 1;28(13):2481–2493. doi: 10.1093/nar/28.13.2481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Vialard J. E., Gilbert C. S., Green C. M., Lowndes N. F. The budding yeast Rad9 checkpoint protein is subjected to Mec1/Tel1-dependent hyperphosphorylation and interacts with Rad53 after DNA damage. EMBO J. 1998 Oct 1;17(19):5679–5688. doi: 10.1093/emboj/17.19.5679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Wach A., Brachat A., Pöhlmann R., Philippsen P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast. 1994 Dec;10(13):1793–1808. doi: 10.1002/yea.320101310. [DOI] [PubMed] [Google Scholar]
  68. Wang H., Guan J., Wang H., Perrault A. R., Wang Y., Iliakis G. Replication protein A2 phosphorylation after DNA damage by the coordinated action of ataxia telangiectasia-mutated and DNA-dependent protein kinase. Cancer Res. 2001 Dec 1;61(23):8554–8563. [PubMed] [Google Scholar]
  69. Wilson S., Tavassoli M., Watts F. Z. Schizosaccharomyces pombe rad32 protein: a phosphoprotein with an essential phosphoesterase motif required for repair of DNA double strand breaks. Nucleic Acids Res. 1998 Dec 1;26(23):5261–5269. doi: 10.1093/nar/26.23.5261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Wilson S., Warr N., Taylor D. L., Watts F. Z. The role of Schizosaccharomyces pombe Rad32, the Mre11 homologue, and other DNA damage response proteins in non-homologous end joining and telomere length maintenance. Nucleic Acids Res. 1999 Jul 1;27(13):2655–2661. doi: 10.1093/nar/27.13.2655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Wolkow Tom D., Enoch Tamar. Fission yeast Rad26 is a regulatory subunit of the Rad3 checkpoint kinase. Mol Biol Cell. 2002 Feb;13(2):480–492. doi: 10.1091/mbc.01-03-0104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Wotton D., Shore D. A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae. Genes Dev. 1997 Mar 15;11(6):748–760. doi: 10.1101/gad.11.6.748. [DOI] [PubMed] [Google Scholar]
  73. Zhu X. D., Küster B., Mann M., Petrini J. H., de Lange T. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat Genet. 2000 Jul;25(3):347–352. doi: 10.1038/77139. [DOI] [PubMed] [Google Scholar]
  74. al-Khodairy F., Carr A. M. DNA repair mutants defining G2 checkpoint pathways in Schizosaccharomyces pombe. EMBO J. 1992 Apr;11(4):1343–1350. doi: 10.1002/j.1460-2075.1992.tb05179.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. al-Khodairy F., Fotou E., Sheldrick K. S., Griffiths D. J., Lehmann A. R., Carr A. M. Identification and characterization of new elements involved in checkpoint and feedback controls in fission yeast. Mol Biol Cell. 1994 Feb;5(2):147–160. doi: 10.1091/mbc.5.2.147. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES