Roles of the checkpoint sensor clamp Rad9-Rad1-Hus1 (911)-complex and the clamp loaders Rad17-RFC and Ctf18-RFC in Schizosaccharomyces pombe telomere maintenance

Cell Cycle

Volumn 9, Issue 11, 2010, Pages 2237-2248

  Khair, Lyne ^a   Chang, Ya Ting ^a   Subramanian, Lakxmi ^a   Russell, Paul ^b   Nakamura, Toru M ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Checkpoint; Ctf18; Rad17; Rad9 Rad1 Hus1; Telomere

Indexed keywords

HYBRID PROTEIN; NUCLEIC ACID BINDING PROTEIN; PROTEIN HUS1; PROTEIN POT1; PROTEIN RAD1; PROTEIN RAD17; PROTEIN RAD9; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; DNA BINDING; NONHUMAN; PROTEIN DOMAIN; SCHIZOSACCHAROMYCES POMBE; TELOMERE;

EUKARYOTA; SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 77953600547     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.11.11920     Document Type: Article

References (69)

1. Verdun RE, Karlseder J. Replication and protection of telomeres. Nature 2007; 447:924-31.
2. Palm W, de Lange T. How shelterin protects mammalian telomeres. Annu Rev Genet 2008; 42:301-34.
3. Miyoshi T, Kanoh J, Saito M, Ishikawa F. Fission yeast Pot1-Tpp1 protects telomeres and regulates telomere length. Science 2008; 320:1341-4. (Pubitemid 351929470)
4. Hockemeyer D, Palm W, Else T, Daniels JP, Takai KK, Ye JZ, et al. Telomere protection by mammalian Pot1 requires interaction with Tpp1. Nat Struct Mol Biol 2007; 14:754-61. (Pubitemid 47220056)
5. Baumann P, Cech TR. Pot1, the putative telomere endbinding protein in fission yeast and humans. Science 2001; 292:1171-5. (Pubitemid 32440940)
6. Xin H, Liu D, Wan M, Safari A, Kim H, Sun W, et al. TPP1 is a homologue of ciliate TEBP-β and interacts with POT1 to recruit telomerase. Nature 2007; 445:559-62. (Pubitemid 46197638)
7. Wang F, Podell ER, Zaug AJ, Yang Y, Baciu P, Cech TR, et al. The POT1-TPP1 telomere complex is a telomerase processivity factor. Nature 2007; 445:506-10. (Pubitemid 46197626)
8. Autexier C, Lue NF. The structure and function of telomerase reverse transcriptase. Annu Rev Biochem 2006; 75:493-517. (Pubitemid 44118041)
9. Zappulla DC, Cech TR. Yeast telomerase RNA: a flexible scaffold for protein subunits. Proc Natl Acad Sci USA 2004; 101:10024-9.
10. Nakamura TM, Morin GB, Chapman KB, Weinrich SL, Andrews WH, Lingner J, et al. Telomerase catalytic subunit homologs from fission yeast and human. Science 1997; 277:955-9.
11. Webb CJ, Zakian VA. Identification and characterization of the Schizosaccharomyces pombe TER1 telomerase RNA. Nat Struct Mol Biol 2008; 15:34-42.
12. Leonardi J, Box JA, Bunch JT, Baumann P. TER1, the RNA subunit of fission yeast telomerase. Nat Struct Mol Biol 2008; 15:26-33.
13. Tomita K, Cooper JP. Fission yeast Ccq1 is telomerase recruiter and local checkpoint controller. Genes Dev 2008; 22:3461-74.
14. ATR promote telomere protection and telomerase recruitment. PLoS Genet 2009; 5:1000622.
15. Sugiyama T, Cam HP, Sugiyama R, Noma K, Zofall M, Kobayashi R, et al. SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 2007; 128:491-504.
16. Longhese MP. DNA damage response at functional and dysfunctional telomeres. Genes Dev 2008; 22:125-40.
17. Lydall D. Taming the tiger by the tail: modulation of DNA damage responses by telomeres. EMBO J 2009; 28:2174-87.
18. Vespa L, Couvillion M, Spangler E, Shippen DE. ATM and ATR make distinct contributions to chromosome end protection and the maintenance of telomeric DNA in Arabidopsis. Genes Dev 2005; 19:2111-5. (Pubitemid 41330313)
19. Francia S, Weiss R, Hande M, Freire R, d'Adda di Fagagna F. Telomere and Telomerase Modulation by the Mammalian Rad9/Rad1/Hus1 DNA-Damage- Checkpoint Complex. Curr Biol 2006; 16:1551-8.
20. Ahmed S, Hodgkin J. MRT-2 checkpoint protein is required for germline immortality and telomere replication in C. elegans. Nature 2000; 403:159-64.
21. Ritchie KB, Mallory JC, Petes TD. 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; 19:6065-75.
22. Nakamura TM, Moser BA, Russell P. Telomere binding of checkpoint sensor and DNA repair proteins contributes to maintenance of functional fission yeast telomeres. Genetics 2002; 161:1437-52. (Pubitemid 35014747)
23. Boerckel J, Walker D, Ahmed S. The Caenorhabditis elegans Rad17 homolog HPR-17 is required for telomere replication. Genetics 2007; 176:703-9.
24. Moser BA, Subramanian L, Chang YT, Noguchi C, Noguchi E, Nakamura TM. Differential arrival of leading and lagging strand DNA polymerases at fission yeast telomeres. EMBO J 2009; 28:810-20.
25. 2 of the cell cycle. Mol Cell 2005; 20:551-61.
26. Verdun RE, Karlseder J. The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 2006; 127:709-20.
27. Dahlén M, Olsson T, Kanter-Smoler G, Ramne A, Sunnerhagen P. Regulation of telomere length by checkpoint genes in Schizosaccharomyces pombe. Mol Biol Cell 1998; 9:611-21.
28. Mayer ML, Gygi SP, Aebersold R, Hieter P. Identification of RFC(Ctf18p, Ctf8p, Dcc1p): an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae. Mol Cell 2001; 7:959-70.
29. Evans SK, Lundblad V. Est1 and Cdc13 as comediators of telomerase access. Science 1999; 286:117-20.
30. Grandin N, Damon C, Charbonneau M. Cdc13 cooperates with the yeast Ku proteins and Stn1 to regulate telomerase recruitment. Mol Cell Biol 2000; 20:8397-408.
31. Pennock E, Buckley K, Lundblad V. Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 2001; 104:387-96.
32. Lei M, Podell ER, Baumann P, Cech TR. DNA selfrecognition in the structure of Pot1 bound to telomeric single-stranded DNA. Nature 2003; 426:198-203.
33. Mitton-Fry RM, Anderson EM, Hughes TR, Lundblad V, Wuttke DS. Conserved structure for single-stranded telomeric DNA recognition. Science 2002; 296:145-7.
34. Naito T, Matsuura A, Ishikawa F. Circular chromosome formation in a fission yeast mutant defective in two ATM homologues. Nat Genet 1998; 20:203-6.
35. Lei M, Baumann P, Cech TR. Cooperative binding of single-stranded telomeric DNA by the Pot1 protein of Schizosaccharomyces pombe. Biochemistry 2002; 41:14560-8.
36. Chahwan C, Nakamura TM, Sivakumar S, Russell P, Rhind N. The fission yeast Rad32 (Mre11)-Rad50- Nbs1 complex is required for the S-phase DNA damage checkpoint. Mol Cell Biol 2003; 23:6564-73. (Pubitemid 37075767)
37. Rouse J, Jackson SP. Lcd1p recruits Mec1p to DNA lesions in vitro and in vivo. Mol Cell 2002; 9:857-69. (Pubitemid 34454895)
38. Falck J, Coates J, Jackson SP. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005; 434:605-11.
39. ATM to telomeres in fission yeast. PLoS Genet 2010; 6:1000839.
40. Mordes DA, Nam EA, Cortez D. Dpb11 activates the Mec1-Ddc2 complex. Proc Natl Acad Sci USA 2008; 105:18730-4.
41. Mordes DA, Glick GG, Zhao R, Cortez D. TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes Dev 2008; 22:1478-89. (Pubitemid 351793082)
42. Sohn SY, Cho Y. Crystal structure of the human Rad9- Hus1-Rad1 clamp. J Mol Biol 2009; 390:490-502.
43. Doré AS, Kilkenny ML, Rzechorzek NJ, Pearl LH. Crystal structure of the Rad9-Rad1-Hus1 DNA damage checkpoint complex - implications for clamp loading and regulation. Mol Cell 2009; 34:735-45.
44. Kanoh J, Francesconi S, Collura A, Schramke V, Ishikawa F, Baldacci G, et al. The fission yeast spSet1p is a histone H3-K4 methyltransferase that functions in telomere maintenance and DNA repair in an ATM kinase Rad3-dependent pathway. J Mol Biol 2003; 326:1081-94. (Pubitemid 36263384)
45. Hofmann ER, Milstein S, Boulton SJ, Ye M, Hofmann JJ, Stergiou L, et al. Caenorhabditis elegans HUS-1 is a DNA damage checkpoint protein required for genome stability and EGL-1-mediated apoptosis. Curr Biol 2002; 12:1908-18.
46. Ellison V, Stillman B. Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5′ recessed DNA. PLoS Biol 2003; 1:33. (Pubitemid 39112165)
47. Bermudez VP, Lindsey-Boltz LA, Cesare AJ, Maniwa Y, Griffith JD, Hurwitz J, et al. Loading of the human 9-1-1 checkpoint complex onto DNA by the checkpoint clamp loader hRad17-replication factor C complex in vitro. Proc Natl Acad Sci USA 2003; 100:1633-8.
48. Majka J, Burgers PM. Yeast Rad17/Mec3/Ddc1: a sliding clamp for the DNA damage checkpoint. Proc Natl Acad Sci USA 2003; 100:2249-54. (Pubitemid 36297485)
49. Naiki T, Kondo T, Nakada D, Matsumoto K, Sugimoto K. Chl12 (Ctf18) forms a novel replication factor C-related complex and functions redundantly with Rad24 in the DNA replication checkpoint pathway. Mol Cell Biol 2001; 21:5838-45. (Pubitemid 32737801)
50. Croy JE, Altschuler SE, Grimm NE, Wuttke DS. Nonadditivity in the recognition of single-stranded DNA by the Schizosaccharomyces pombe protection of telomeres 1 DNA-binding domain, Pot1-DBD. Biochemistry 2009; 48:6864-75.
51. Croy JE, Podell ER, Wuttke DS. A new model for Schizosaccharomyces pombe telomere recognition: the telomeric single-stranded DNA-binding activity of Pot11-389. J Mol Biol 2006; 361:80-93.
52. Majka J, Niedziela-Majka A, Burgers PM. The checkpoint clamp activates Mec1 kinase during initiation of the DNA damage checkpoint. Mol Cell 2006; 24:891-901. (Pubitemid 44960097)
53. Caspari T, Dahlen M, Kanter-Smoler G, Lindsay HD, Hofmann K, Papadimitriou K, et al. Characterization of Schizosaccharomyces pombe Hus1: a PCNA-related protein that associates with Rad1 and Rad9. Mol Cell Biol 2000; 20:1254-62.
54. + checkpoint gene. J Biol Chem 1998; 273:18340-6.
55. Rauen M, Burtelow MA, Dufault VM, Karnitz LM. The human checkpoint protein hRad17 interacts with the PCNA-like proteins hRad1, hHus1 and hRad9. J Biol Chem 2000; 275:29767-71. (Pubitemid 32043860)
56. Burtelow MA, Roos-Mattjus PM, Rauen M, Babendure JR, Karnitz LM. Reconstitution and molecular analysis of the hRad9-hHus1-hRad1 (9-1-1) DNA damage responsive checkpoint complex. J Biol Chem 2001; 276:25903-9. (Pubitemid 37412795)
57. Majka J, Burgers PM. Function of Rad17/Mec3/Ddc1 and its partial complexes in the DNA damage checkpoint. DNA Repair (Amst) 2005; 4:1189-94. (Pubitemid 41316596)
58. Wolkow TD, Enoch T. Fission yeast Rad26 responds to DNA damage independently of Rad3. BMC Genet 2003; 4:6. (Pubitemid 38671560)
59. Longhese MP, Paciotti V, Neecke H, Lucchini G. Checkpoint proteins influence telomeric silencing and length maintenance in budding yeast. Genetics 2000; 155:1577-91. (Pubitemid 30626380)
60. Corda Y, Schramke V, Longhese MP, Smokvina T, Paciotti V, Brevet V, et al. Interaction between Set1p and checkpoint protein Mec3p in DNA repair and telomere functions. Nat Genet 1999; 21:204-8. (Pubitemid 29070368)
61. Grandin N, Damon C, Charbonneau M. Cdc13 prevents telomere uncapping and Rad50-dependent homologous recombination. EMBO J 2001; 20:6127-39. (Pubitemid 33049287)
62. Zhang H, Zhu Z, Vidanes G, Mbangkollo D, Liu Y, Siede W. Characterization of DNA damage-stimulated self-interaction of Saccharomyces cerevisiae checkpoint protein Rad17p. J Biol Chem 2001; 276:26715-23.
63. Merkle CJ, Karnitz LM, Henry-Sánchez JT, Chen J. Cloning and characterization of hCTF18, hCTF8 and hDCC1. Human homologs of a Saccharomyces cerevisiae complex involved in sister chromatid cohesion establishment. J Biol Chem 2003; 278:30051-6.
64. Kim J, Robertson K, Mylonas KJ, Gray FC, Charapitsa I, MacNeill SA. Contrasting effects of Elg1-RFC and Ctf18-RFC inactivation in the absence of fully functional RFC in fission yeast. Nucleic Acids Res 2005; 33:4078-89. (Pubitemid 41487268)
65. tf18 and the Swi1-Swi3 complex function in separate and redundant pathways required for the stabilization of replication forks to facilitate sister chromatid cohesion in Schizosaccharomyces pombe. Mol Biol Cell 2008; 19:595-607.
66. Hanna JS, Kroll ES, Lundblad V, Spencer FA. Saccharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion. Mol Cell Biol 2001; 21:3144-58.
67. Alfa C, Fantes P, Hyams J, McLoed M, Warbrick E. Experiments with Fission Yeast. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press 1993.
68. Nakamura TM, Cooper JP, Cech TR. Two modes of survival of fission yeast without telomerase. Science 1998; 282:493-6.
69. Khair L, Subramanian L, Moser BA, Nakamura TM. Roles of heterochromatin and telomere proteins in regulation of fission yeast telomere recombination and telomerase recruitment. J Biol Chem 2009; 285:5327-37.