Human Rif1, ortholog of a yeast telomeric protein, is regulated by ATM and 53BP1 and functions in the S-phase checkpoint

Genes and Development

Volumn 18, Issue 17, 2004, Pages 2108-2119

  Silverman, Joshua ^a   Takai, Hiroyuki ^a   Buonomo, Sara B C ^a   Eisenhaber, Frank ^b   De Lange, Titia ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

53BP1; ATM; Checkpoint; Nbs1; Rif1; Telomere

Indexed keywords

ATM PROTEIN; BRCA1 PROTEIN; CHECKPOINT KINASE 2; DNA; GENE PRODUCT; MRE11 PROTEIN; NIBRIN; PROTEIN 53BP1; RAP1 INTERACTING FACTOR 1; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA STRAND BREAKAGE; GENE CONTROL; HUMAN; HUMAN CELL; MAMMAL; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RADIOSENSITIVITY; SACCHAROMYCES CEREVISIAE; TELOMERE;

BASE SEQUENCE; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELLS, CULTURED; DNA DAMAGE; DNA REPLICATION; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOBLOTTING; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; S PHASE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERE; TELOMERE-BINDING PROTEINS; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS; ULTRAVIOLET RAYS;

MAMMALIA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 3543064379     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1216004     Document Type: Article

References (72)

1. Abraham, R.T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes & Dev. 15: 2177-2196.
2. Adams, I.R. and McLaren, A. 2004. Identification and characterization of mRif1: A mouse telomere-associated protein highly expressed in germ cells and embryo-derived pluripotent stem cells. Dev. Dyn. 229: 733-744.
3. Bailey, S.M., Meyne, J., Chen, D.J., Kurimasa, A., Li, G.C., Lehnert, B.E., and Goodwin, E.H. 1999. DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc. Natl. Acad. Sci. 96: 14899-14904.
4. Bakkenist, C.J. and Kastan, M.B. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499-506.
5. Chan, S.W., Chang, J., Prescott, J., and Blackburn, E.H. 2001. Altering telomere structure allows telomerase to act in yeast lacking ATM kinases. Curr. Biol. 11: 1240-1250.
6. Cortez, D., Guntuku, S., Qin, J., and Elledge, S.J. 2001. ATR and ATRIP: Partners in checkpoint signaling. Science 294: 1713-1716.
7. Craven, R.J. and Petes, T.D. 1999. Dependence of the regulation of telomere length on the type of subtelomeric repeat in the yeast Saccharomyces cerevisiae. Genetics 152: 1531-1541.
8. d'Adda di Fagagna, F., Reaper, P.M., Clay-Farrace, L., Fiegler, H., Carr, P., Von Zglinicki, T., Saretzki, G., Carter, N.P., and Jackson, S.P. 2003. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426: 194-198.
9. D'Andrea, A.D. and Grompe, M. 2003. The Fanconi anaemia/BRCA pathway. Nat. Rev. Cancer 3: 23-34.
10. de Lange, T. 2002. Protection of mammalian telomeres. Oncogene 21: 532-540.
11. -. 2004. T-loops and the origin of telomeres. Nat. Rev. Mol. Cell Biology 5: 323-329.
12. DiTullio Jr., R.A., Mochan, T.A., Venere, M., Bartkova, J., Sehested, M., Bartek, J., and Halazonetis, T.D. 2002. 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat. Cell Biol. 4: 998-1002.
13. Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498.
14. Falck, J., Mailand, N., Syljuasen, R.G., Bartek, J., and Lukas, J. 2001. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 410: 842-847.
15. Falck, J., Petrini, J.H., Williams, B.R., Lukas, J., and Bartek, J. 2002. The DNA damage-dependent intra-S phase checkpoint is regulated by parallel pathways. Nat. Genet. 30: 290-294.
16. Ferreira, M.G., Miller, K.M., and Cooper, J.P. 2004. Indecent exposure: When telomeres become uncapped. Mol. Cell 13: 7-18.
17. Ganesan, S., Silver, D.P., Greenberg, R.A., Avni, D., Drapkin, R., Miron, A., Mok, S.C., Randrianarison, V., Brodie, S., Salstrom, J., et al. 2002. BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell 111: 393-405.
18. Gatei, M., Young, D., Cerosaletti, K.M., Desai-Mehta, A., Spring, K., Kozlov, S., Lavin, M.F., Gatti, R.A., Concannon, P., and Khanna, K. 2000. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat. Genet. 25: 115-119.
19. Haaf, T., Golub, E.I., Reddy, G., Radding, C.M., and Ward, D.C. 1995. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc. Natl. Acad. Sci. 92: 2298-2302.
20. Hannan, M.A., Hellani, A., Al-Khodairy, F.M., Kunhi, M., Siddiqui, Y., Al-Yussef, N., Pangue-Cruz, N., Siewertsen, M., Al-Ahdal, M.N., and Aboussekhra, A. 2002. Deficiency in the repair of UV-induced DNA damage in human skin fibroblasts compromised for the ATM gene. Carcinogenesis 23: 1617-1624.
21. Hardy, C.F., Sussel, L., and Shore, D. 1992. A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation. Genes & Dev. 6: 801-814.
22. Heinloth, A.N., Shackelford, R.E., Innes, C.L., Bennett, L., Li, L., Amin, R.P., Sieber, S.O., Flores, K.G., Bushel, P.R., and Paules, R.S. 2003. ATM-dependent and -independent gene expression changes in response to oxidative stress, γ irradiation, and UV irradiation. Radiat. Res. 160: 273-290.
23. Henson, J.D., Neumann, A.A., Yeager, T.R., and Reddel, R.R. 2002. Alternative lengthening of telomeres in mammalian cells. Oncogene 21: 598-610.
24. Jallepalli, P.V., Lengauer, C., Vogelstein, B., and Bunz, F. 2003. The Chk2 tumor suppressor is not required for p53 responses in human cancer cells. J. Biol. Chem. 278: 20475-20479.
25. Jaspers, N.G., de Wit, J., Regulski, M.R., and Bootsma, D. 1982. Abnormal regulation of DNA replication and increased lethality in ataxia telangiectasia cells exposed to carcinogenic agents. Cancer Res. 42: 335-341.
26. Kanoh, J. and Ishikawa, F. 2001. spRap1 and spRif1, recruited to telomeres by Taz1, are essential for telomere function in fission yeast. Curr. Biol. 11: 1624-1630.
27. Karlseder, J., Broccoli, D., Dai, Y., Hardy, S., and de Lange, T. 1999. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283: 1321-1325.
28. Kastan, M.B. and Lim, D.S. 2000. The many substrates and functions of ATM. Nat. Rev. Mol. Cell. Biol. 1: 179-186.
29. Kim, S.T., Xu, B., and Kastan, M.B. 2002. Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes & Dev. 16: 560-570.
30. Kraakman-van der Zwet, M., Overkamp, W.J., Friedl, A.A., Klein, B., Verhaegh, G.W., Jaspers, N.G., Midro, A.T., Eckardt-Schupp, F., Lohman, P.H., and Zdzienicka, M.Z. 1999. Immortalization and characterization of Nijmegen Breakage syndrome fibroblasts. Mutat. Res. 434: 17-27.
31. Li, B., Oestreich, S., and de Lange, T. 2000. Identification of human Rap1: Implications for telomere evolution. Cell 101: 471-483.
32. Lim, D.S., Kim, S.T., Xu, B., Maser, R.S., Lin, J., Petrini, J.H., and Kastan, M.B. 2000. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404: 613-617.
33. Marcand, S., Gilson, E., and Shore, D. 1997. A protein-counting mechanism for telomere length regulation in yeast Science 275: 986-990.
34. Maser, R.S., Bressan, D.A., and Petrini, J. 2001. The Mre11-Rad50 complex: Diverse functions in the cellular DNA damage response. In DNA damage and repair (eds. M.F. Hoekstra and J.A. Nickoloff), pp. 147-172. Humana Press, Totowa, NJ.
35. Mirzoeva, O.K. and Petrini, J.H. 2001. DNA damage-dependent nuclear dynamics of the Mre11 complex. Mol. Cell. Biol. 21: 281-288.
36. Mochan, T.A., Venere, M., DiTullio Jr., R.A., and Halazonetis, T.D. 2003. 53BP1 and NFBD1/MDC1-Nbs1 function in parallel interacting pathways activating ataxia-telangiectasia mutated (ATM) in response to DNA damage. Cancer Res. 63: 8586-8591.
37. Myung, K., Chen, C., and Kolodner, R.D. 2001a. Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature 411: 1073-1076.
38. Myung, K., Datta, A., and Kolodner, R.D. 2001b. Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell 104: 397-408.
39. Novina, C.D., Murray, M.F., Dykxhoorn, D.M., Beresford, P.J., Riess, J., Lee, S.K., Collman, R.G., Lieberman, J., Shankar, P., and Sharp, P.A. 2002. siRNA-directed inhibition of HIV-1 infection. Nat. Med. 8: 681-686.
40. 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., and Dixon, K. 2001. UV-induced hyperphosphorylation of replication protein a depends on DNA replication and expression of ATM protein. Mol. Biol. Cell 12: 1199-1213.
41. O'Driscoll, M., Ruiz-Perez, V.L., Woods, C.G., Jeggo, P.A., and Goodship, J.A. 2003. A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat. Genet. 33: 497-501.
42. Osborn, A.J., Elledge, S.J., and Zou, L. 2002. Checking on the fork: The DNA-replication stress-response pathway. Trends Cell. Biol. 12: 509-516.
43. Ouellette, M.M., McDaniel, L.D., Wright, W.E., Shay, J.W., and Schultz, R.A. 2000. The establishment of telomerase-immortalized cell lines representing human chromosome instability syndromes. Hum. Mol. Genet. 9: 403-411.
44. Painter, R.B. and Young, B.R. 1980. Radiosensitivity in ataxia-telangiectasia: A new explanation. Proc. Natl. Acad. Sci. 77: 7315-7317.
45. Petrini, J. and Stracker, T. 2003. The cellular response to DNA double strand breaks: Defining the sensors and mediators. Trends Cell. Biol. 13: 458-462.
46. Rappold, I., Iwabuchi, K., Date, T., and Chen, J. 2001. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J. Cell. Biol. 153: 613-620.
47. Shiloh, Y. 2003. ATM and related protein kinases: Safeguarding genome integrity. Nat. Rev. Cancer 3: 155-168.
48. Smogorzewska, A. and de Lange, T. 2004. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem. 73: 177-208.
49. Smogorzewska, A., van Steensel, B., Bianchi, A., Oelmann, S., Schaefer, M.R., Schnapp, G., and de Lange, T. 2000. Control of human telomere length by TRF1 and TRF2. Mol. Cell. Biol. 20: 1659-1668.
50. Smogorzewska, A., Karlseder, J., Holtgreve-Grez, H., Jauch, A., and de Lange, T. 2002. DNA ligase IV-dependent NHEJ of deprotected mammalian telomeres in G1 and G2. Curr. Biol. 12: 1635.
51. Stewart, G.S., Maser, R.S., Stankovic, T., Bressan, D.A., Kaplan, M.I., Jaspers, N.G., Raams, A., Byrd, P.J., Petrini, J.H., and Taylor, A.M. 1999. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 99: 577-587.
52. Takai, H., Smogorzewska, A., and de Lange, T. 2003. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13: 1549-1556.
53. Taniguchi, T., Garcia-Higuera, I., Xu, B., Andreassen, P.R., Gregory, R.C., Kim, S.T., Lane, W.S., Kastan, M.B., and D'Andrea, A.D. 2002. Convergence of the fanconi anemia and ataxia telangiectasia signaling pathways. Cell 109: 459-472.
54. Taylor, A.M., Harnden, D.G., Arlett, C.F., Harcourt, S.A., Lehmann, A.R., Stevens, S., and Bridges, B.A. 1975. Ataxia telangiectasia: A human mutation with abnormal radiation sensitivity. Nature 258: 427-429.
55. Teixeira, M.T., Arneric, M., Sperisen, P., and Lingner, J. 2004. Telomere length homeostasis is achieved via a switch between telomerase-extendible and -nonextendible states. Cell 117: 323-335.
56. van Steensel, B. and de Lange, T. 1997. Control of telomere length by the human telomeric protein TRF1 Nature 385: 740-743.
57. van Steensel, B., Smogorzewska, A., and de Lange, T. 1998. TRF2 protects human telomeres from end-to-end fusions. Cell 92: 401-413.
58. Wang, B., Matsuoka, S., Carpenter, P.B., and Elledge, S.J. 2002. 53BP1, a mediator of the DNA damage checkpoint. Science 298: 1435-1438.
59. Ward, I.M., Minn, K., van Deursen, J., and Chen, J. 2003. p53 binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 23: 2556-2563.
60. Wong, K.K., Maser, R.S., Bachoo, R.M., Menon, J., Carrasco, D.R., Gu, Y., Alt, F.W., and DePinho, R.A. 2003. Telomere dysfunction and Atm deficiency compromises organ homeostasis and accelerates ageing. Nature 421: 643-648.
61. Wotton, D. and Shore, D. 1997. A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae. Genes & Dev. 11: 748-760.
62. Wu, X., Ranganathan, V., Weisman, D.S., Heine, W.F., Ciccone, D.N., O'Neill, T.B., Crick, K.E., Pierce, K.A., Lane, W.S., Rathbun, G., et al. 2000. ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature 405: 477-482.
63. Xu, B., Kim, S., and Kastan, M.B. 2001. Involvement of Brca1 in S-phase and G(2)-phase checkpoints after ionizing irradiation. Mol. Cell. Biol. 21: 3445-3450.
64. Xu, B., Kim, S.T., Lim, D.S., and Kastan, M.B. 2002a. Two molecularly distinct G(2)/M checkpoints are induced by ionizing irradiation. Mol. Cell. Biol. 22: 1049-1059.
65. Xu, B., O'Donnell, A.H., Kim, S.T., and Kastan, M.B. 2002b. Phosphorylation of serine 1387 in Brcal is specifically required for the Atm-mediated S-phase checkpoint after ionizing irradiation. Cancer Res. 62: 4588-4591.
66. Yazdi, P.T., Wang, Y., Zhao, S., Patel, N., Lee, E.Y., and Qin, J. 2002. SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes & Dev. 16: 571-582.
67. Yeager, T.R., Neumann, A.A., Englezou, A., Huschtscha, L.I., Noble, J.R., and Reddel, R.R. 1999. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59: 4175-4179.
68. Zhao, S., Weng, Y.C., Yuan, S.S., Lin, Y.T., Hsu, H.C., Lin, S.C., Gerbino, E., Song, M.H., Zdzienicka, M.Z., Gatti, R.A., et al. 2000. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature 405: 473-477.
69. Zhou, B.B. and Elledge, S.J. 2000. The DNA damage response: Putting checkpoints in perspective. Nature 408: 433-439.
70. Zhu, X.D., Kuster, B., Mann, M., Petrini, J.H., and de Lange, T. 2000. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25: 347-352.
71. Zhu, X.D., Niedernhofer, L., Kuster, B., Mann, M., Hoeijmakers, J.H., and de Lange, T. 2003. ERCC1/XPF removes the 3′ overhang from uncapped telomeres and represses formation of telomeric DNA-containing double minute chromosomes. Mol. Cell 12: 1489-1498.
72. Zou, L. and Elledge, S.J. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.