Increased common fragile site expression, cell proliferation defects, and apoptosis following conditional inactivation of mouse Hus1 in primary cultured cells

Molecular Biology of the Cell

Volumn 18, Issue 3, 2007, Pages 1044-1055

  Zhu, Min ^a   Weiss, Robert S ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; DOUBLE STRANDED DNA; HISTONE H2AX; MUTANT PROTEIN; PROTEIN P53;

ADENOVIRUS; ALLELE; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE S PHASE; CELL PROLIFERATION; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CONTROLLED STUDY; DNA REPLICATION; DNA STRAND BREAKAGE; EMBRYO; FIBROBLAST CULTURE; GENE; GENE CONTROL; GENE DELETION; GENE DISRUPTION; GENE FUNCTION; GENE INACTIVATION; GENE LOCUS; GENETIC ASSOCIATION; GENOTYPE PHENOTYPE CORRELATION; HUS1 GENE; KNOCKOUT GENE; LOXP SITE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TUMOR SUPPRESSOR GENE;

ANIMALS; APOPTOSIS; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; CHROMOSOME ABERRATIONS; CHROMOSOME FRAGILE SITES; FIBROBLASTS; GENE DELETION; HISTONES; HUMANS; INTEGRASES; MICE; PHENOTYPE; PHOSPHORYLATION; RECOMBINATION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

ADENOVIRIDAE;

EID: 33947145194     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-10-0957     Document Type: Article

References (78)

1. Arlt, M. F., Durkin, S. G., Ragland, R. L., and Glover, T. W. (2006). Common fragile sites as targets for chromosome rearrangements. DNA Repair 5, 1126-1135.
2. Arlt, M. F., Xu, B., Durkin, S. G., Casper, A. M., Kastan, M. B., and Glover, T. W. (2004). BRCA1 is required for common-fragile-site stability via its G2/M checkpoint function. Mol. Cell. Biol. 24, 6701-6709.
3. Bakkenist, C. J., and Kastan, M. B. (2004). Initiating cellular stress responses. Cell 118, 9-17.
4. Bao, S., Lu, T., Wang, X., Zheng, H., Wang, L. E., Wei, Q., Hittelman, W. N., and Li, L. (2004). Disruption of the Rad9/Rad1/Hus1 (9-1-1) complex leads to checkpoint signaling and replication defects. Oncogene 23, 5586-5593.
5. Bao, S., Tibbetts, R. S., Brumbaugh, K. M., Fang, Y., Richardson, D. A., Ali, A., Chen, S. M., Abraham, R. T., and Wang, X. F. (2001). ATR/ATM-mediated phosphorylation of human Rad17 is required for genotoxic stress responses. Nature 411, 969-974.
6. Blasco, M. A., Lee, H. W., Hande, M. P., Samper, E., Lansdorp, P. M., DePinho, R. A., and Greider, C. W. (1997). Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91, 25-34.
7. Brown, E. J., and Baltimore, D. (2000). ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14, 397-402.
8. Brown, E. J., and Baltimore, D. (2003). Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev. 17, 615-628.
9. Budzowska, M., et al. (2004). Mutation of the mouse Rad17 gene leads to embryonic lethality and reveals a role in DNA damage-dependent recombination. EMBO J. 23, 3548-3558.
10. Casper, A. M., Nghiem, P., Arlt, M. F., and Glover, T. W. (2002). ATR regulates fragile site stability. Cell 111, 779-789.
11. Cha, R. S., and Kleckner, N. (2002). ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297, 602-606.
12. Chang, D. Y., and Lu, A. L. (2005). Interaction of checkpoint proteins Hus1/ Rad1/Rad9 with DNA base excision repair enzyme MutY homolog in fission yeast, Schizosaccharomyces pombe. J. Biol. Chem. 280, 408-417.
13. Cimprich, K. A. (2003). Fragile sites: breaking up over a slowdown. Curr. Biol. 13, R231-R233.
14. Cortez, D., Guntuku, S., Qin, J., and Elledge, S. J. (2001). ATR and ATRIP: partners in checkpoint signaling. Science 294, 1713-1716.
15. Dart, D. A., Adams, K. E., Akerman, I., and Lakin, N. D. (2004). Recruitment of the cell cycle checkpoint kinase ATR to chromatin during S-phase. J. Biol. Chem. 279, 16433-16440.
16. de Klein, A., Muijtjens, M., van Os, R., Verhoeven, Y., Smit, B., Carr, A. M., Lehmann, A. R., and Hoeijmakers, J. H. (2000). Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10, 479-482.
17. Durkin, S. G., Arlt, M. F., Howlett, N. G., and Glover, T. W. (2006). Depletion of CHK1, but not CHK2, induces chromosomal instability and breaks at common fragile sites. Oncogene 25, 4381-4388.
18. Friedrich-Heineken, E., Toueille, M., Tannler, B., Burki, C., Ferrari, E., Hottiger, M. O., and Hubscher, U. (2005). The two DNA clamps Rad9/Rad1/Hus1 complex and proliferating cell nuclear antigen differentially regulate flap endonuclease 1 activity. J. Mol. Biol. 353, 980-989.
19. Glover, T. W., Arlt, M. F., Casper, A. M., and Durkin, S. G. (2005). Mechanisms of common fragile site instability. Hum. Mol. Genet. 14, R197-R205.
20. Guo, Z., Kumagai, A., Wang, S. X., and Dunphy, W. G. (2000). Requirement for Atr in phosphorylation of Chk1 and cell cycle regulation in response to DNA replication blocks and UV-damaged DNA in Xenopus egg extracts. Genes Dev. 14, 2745-2756.
21. Harris, S. L., and Levine, A. J. (2005). The p53 pathway: positive and negative feedback loops. Oncogene 24, 2899-2908.
22. Hekmat-Nejad, M., You, Z., Yee, M. C., Newport, J. W., and Cimprich, K. A. (2000). Xenopus ATR is a replication-dependent chromatin-binding protein required for the DNA replication checkpoint. Curr. Biol. 10, 1565-1573.
23. Hopkins, K. M., Auerbach, W., Wang, X. Y., Hande, M. P., Hang, H., Wolgemuth, D. J., Joyner, A. L., and Lieberman, H. B. (2004). Deletion of mouse rad9 causes abnormal cellular responses to DNA damage, genomic instability, and embryonic lethality. Mol. Cell. Biol. 24, 7235-7248.
24. Jacks, T., Remington, L., Williams, B. O., Schmitt, E. M., Halachmi, S., Bronson, R. T., and Weinberg, R. A. (1994). Tumor spectrum analysis in p53-mutant mice. Curr. Biol. 4, 1-7.
25. Jiang, K., Pereira, E., Maxfield, M., Russell, B., Goudelock, D. M., and Sanchez, Y. (2003). Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J. Biol. Chem. 278, 25207-25217.
26. Kai, M., and Wang, T. S. (2003). Checkpoint activation regulates mutagenic translesion synthesis. Genes Dev. 17, 64-76.
27. Kim, J. E., McAvoy, S. A., Smith, D. I., and Chen, J. (2005). Human TopBP1 ensures genome integrity during normal S phase. Mol. Cell. Biol. 25, 10907-10915.
28. Kinzel, B., Hall, J., Natt, F., Weiler, J., and Cohen, D. (2002). Downregulation of Hus1 by antisense oligonucleotides enhances the sensitivity of human lung carcinoma cells to cisplatin. Cancer 94, 1808-1814.
29. Krummel, K. A., Denison, S. R., Calhoun, E., Phillips, L. A., and Smith, D. I. (2002). The common fragile site FRA16D and its associated gene WWOX are highly conserved in the mouse at Fra8E1. Genes Chromosomes Cancer 34, 154-167.
30. Kumari, A., Schultz, N., and Helleday, T. (2004). p53 protects from replication-associated DNA double-strand breaks in mammalian cells. Oncogene 23, 2324-2329.
31. Lee, J., Kumagai, A., and Dunphy, W. G. (2003). Claspin, a Chk1-regulatory protein, monitors DNA replication on chromatin independently of RPA, ATR, and Rad17. Mol. Cell 11, 329-340.
32. Levitt, P. S., Liu, H., Manning, C., and Weiss, R. S. (2005). Conditional inactivation of the mouse Hus1 cell cycle checkpoint gene. Genomics 86, 212-224.
33. 2/M DNA damage checkpoint. Genes Dev. 14, 1448-1459.
34. Liu, S., Bekker-Jensen, S., Mailand, N., Lukas, C., Bartek, J., and Lukas, J. (2006). Claspin operates downstream of TopBP1 to direct ATR signaling towards Chk1 activation. Mol. Cell. Biol. 26, 6056-6064.
35. Loonstra, A., Vooijs, M., Beverloo, H. B., Allak, B. A., van Drunen, E., Kanaar, R., Berns, A., and Jonkers, J. (2001). Growth inhibition and DNA damage induced by Cre recombinase in mammalian cells. Proc. Natl. Acad. Sci. USA 98, 9209-9214.
36. Lopes, M., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Plevani, P., Muzi-Falconi, M., Newlon, C. S., and Foiani, M. (2001). The DNA replication checkpoint stabilizes stalled replication forks. Nature 412, 557-561.
37. Marti, T. M., Hefner, E., Feeney, L., Natale, V., and Cleaver, J. E. (2006). H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 103, 9891-9896.
38. Miao, H., Seiler, J. A., and Burhans, W. C. (2003). Regulation of cellular and SV40 virus origins of replication by Chk1-dependent intrinsic and UVC radiation-induced checkpoints. J. Biol. Chem. 278, 4295-4304.
39. Mitelman, F. (1995). ISCN (1995): An International System for Human Cytogenetic Nomenclature, Basel, Switzerland: S. Karger.
40. Niida, H., Tsuge, S., Katsuno, Y., Konishi, A., Takeda, N., and Nakanishi, M. (2005). Depletion of Chk1 leads to premature activation of Cdc2-cyclin B and mitotic catastrophe. J. Biol. Chem. 280, 39246-39252.
41. Pandita, R. K., et al. (2006). Mammalian Rad9 plays a role in telomere stability, S- and G2-phase-specific cell survival, and homologous recombinational repair. Mol. Cell. Biol. 26, 1850-1864.
42. Parrilla-Castellar, E. R., and Karnitz, L. M. (2003). Cut5 is required for the binding of Atr and DNA polymerase alpha to genotoxin-damaged chromatin. J. Biol. Chem. 278, 45507-45511.
43. Raveendranathan, M., Chattopadhyay, S., Bolon, Y. T., Haworth, J., Clarke, D. J., and Bielinsky, A. K. (2006). Genome-wide replication profiles of S-phase checkpoint mutants reveal fragile sites in yeast. EMBO J. 25, 3627-3639.
44. Roos-Mattjus, P., Hopkins, K. M., Oestreich, A. J., Vroman, B. T., Johnson, K. L., Naylor, S., Lieberman, H. B., and Karnitz, L. M. (2003). Phosphorylation of human Rad9 is required for genotoxin-activated checkpoint signaling. J. Biol. Chem. 278, 24428-24437.
45. Roos-Mattjus, P., Vroman, B. T., Burtelow, M. A., Rauen, M., Eapen, A. K., and Karnitz, L. M. (2002). Genotoxin-induced Rad9-Hus1-Rad1 (9-1-1) chromatin association is an early checkpoint signaling event. J. Biol. Chem. 277, 43809-43812.
46. Rozier, L., El-Achkar, E., Apiou, F., and Debatisse, M. (2004). Characterization of a conserved aphidicolin-sensitive common fragile site at human 4q22 and mouse 6C 1: possible association with an inherited disease and cancer. Oncogene 23, 6872-6880.
47. Sabbioneda, S., Minesinger, B. K., Giannattasio, M., Plevani, P., Muzi-Falconi, M., and Jinks-Robertson, S. (2005). The 9-1-1 checkpoint clamp physically interacts with polζ and is partially required for spontaneous polζ-dependent mutagenesis in Saccharomyces cerevisiae. J. Biol. Chem. 280, 38657-38665.
48. Savage, J. R. (1976). Classification and relationships of induced chromosomal structural changes. J. Med. Genet. 13, 103-122.
49. Schmitt, E., Boutros, R., Froment, C., Monsarrat, B., Ducommun, B., and Dozier, C. (2006). CHK1 phosphorylates CDC25B during the cell cycle in the absence of DNA damage. J. Cell Sci. 119, 4269-4275.
50. Sengupta, S., et al. (2005). Tumor suppressor p53 represses transcription of RECQ4 helicase. Oncogene 24, 1738-1748.
51. Shechter, D., Costanzo, V., and Gautier, J. (2004a). ATR and ATM regulate the timing of DNA replication origin firing. Nat. Cell Biol. 6, 648-655.
52. Shechter, D., Costanzo, V., and Gautier, J. (2004b). Regulation of DNA replication by ATR: signaling in response to DNA intermediates. DNA Repair 3, 901-908.
53. Shi, G., Chang, D. Y., Cheng, C. C., Guan, X., Venclovas, C., and Lu, A. L. (2006). Physical and functional interactions between MutY homolog (MYH) and checkpoint proteins Rad9-Rad1-Hus1. Biochem. J. 400, 53-62.
54. Silver, D. P., and Livingston, D. M. (2001). Self-excising retroviral vectors encoding the Cre recombinase overcome Cre-mediated cellular toxicity. Mol. Cell 8, 233-243.
55. Smirnova, E., Toueille, M., Markkanen, E., and Hubscher, U. (2005). The human checkpoint sensor and alternative DNA clamp Rad9-Rad1-Hus1 modulates the activity of DNA ligase I, a component of the long-patch base excision repair machinery. Biochem. J. 389, 13-17.
56. Sogo, J. M., Lopes, M., and Foiani, M. (2002). Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297, 599-602.
57. Sorensen, C. S., Syljuasen, R. G., Lukas, J., and Bartek, J. (2004). ATR, Claspin and the Rad9-Rad1-Hus1 complex regulate Chk1 and Cdc25A in the absence of DNA damage. Cell Cycle 3, 941-945.
58. Squires, S., Coates, J. A., Goldberg, M., Toji, L. H., Jackson, S. P., Clarke, D. J., and Johnson, R. T. (2004). p53 prevents the accumulation of double-strand DNA breaks at stalled-replication forks induced by UV in human cells. Cell Cycle 3, 1543-1557.
59. Stec, D. E., Davisson, R. L., Haskell, R. E., Davidson, B. L., and Sigmund, C. D. (1999). Efficient liver-specific deletion of a floxed human angiotensinogen transgene by adenoviral delivery of Cre recombinase in vivo. J. Biol. Chem. 274, 21285-21290.
60. Syljuasen, R. G., Sorensen, C. S., Hansen, L. T., Fugger, K., Lundin, C., Johansson, F., Helleday, T., Sehested, M., Lukas, J., and Bartek, J. (2005). Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol. Cell. Biol. 25, 3553-3562.
61. -/- mice. Genes Dev. 14, 1439-1447.
62. Tercero, J. A., and Diffley, J. F. (2001). Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412, 553-557.
63. Todaro, G. J., and Green, H. (1963). Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17, 299-313.
64. Toueille, M., El-Andaloussi, N., Frouin, I., Freire, R., Funk, D., Shevelev, I., Friedrich-Heineken, E., Villani, G., Hottiger, M. O., and Hubscher, U. (2004). The human Rad9/Rad1/Hus1 damage sensor clamp interacts with DNA polymerase beta and increases its DNA substrate utilisation efficiency: implications for DNA repair. Nucleic Acids Res. 32, 3316-3324.
65. Trenz, K., Smith, E., Smith, S., and Costanzo, V. (2006). ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J. 25, 1764-1774.
66. Vermes, I., Haanen, C., Steffens-Nakken, H., and Reutelingsperger, C. (1995). A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods 184, 39-51.
67. Wang, W., Brandt, P., Rossi, M. L., Lindsey-Boltz, L., Podust, V., Fanning, E., Sancar, A., and Bambara, R. A. (2004a). The human Rad9-Rad1-Hus1 checkpoint complex stimulates flap endonuclease 1. Proc. Natl. Acad. Sci. USA 101, 16762-16767.
68. Wang, W., Lindsey-Boltz, L. A., Sancar, A., and Bambara, R. A. (2006a). Mechanism of stimulation of human DNA ligase I by the Rad9-Rad1-Hus1 checkpoint complex. J. Biol. Chem. 281, 20865-20872/
69. Wang, X., Guan, J., Hu, B., Weiss, R. S., Iliakis, G., and Wang, Y. (2004b). Involvement of Hus1 in the chain elongation step of DNA replication after exposure to camptothecin or ionizing radiation. Nucleic Acids Res. 32, 767-775.
70. Wang, X., Hu, B., Weiss, R. S., and Wang, Y. (2006b). The effect of Hus1 on ionizing radiation sensitivity is associated with homologous recombination repair but is independent of nonhomologous end-joining. Oncogene 25, 1980-1983.
71. Wang, X., Zou, L., Zheng, H., Wei, Q., Elledge, S. J., and Li, L. (2003). Genomic instability and endoreduplication triggered by RAD17 deletion. Genes Dev. 17, 965-970.
72. Ward, I. M., and Chen, J. (2001). Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276, 47759-47762.
73. Weiss, R. S., Enoch, T., and Leder, P. (2000). Inactivation of mouse Hus1 results in genomic instability and impaired responses to genotoxic stress. Genes Dev. 14, 1886-1898.
74. Weiss, R. S., Kostrub, C. F., Enoch, T., and Leder, P. (1999). Mouse Hus1, a homolog of the Schizosaccharomyces pombe hus1+ cell cycle checkpoint gene. Genomics 59, 32-39.
75. Weiss, R. S., Leder, P., and Vaziri, C. (2003). Critical role for mouse Hus1 in an S-phase DNA damage cell cycle checkpoint. Mol. Cell. Biol. 23, 791-803.
76. Weiss, R. S., Matsuoka, S., Elledge, S. J., and Leder, P. (2002). Hus1 acts upstream of Chk1 in a mammalian DNA damage response pathway. Curr. Biol. 12, 73-77.
77. You, Z., Kong, L., and Newport, J. (2002). The role of single-stranded DNA and polymerase alpha in establishing the ATR, Hus1 DNA replication checkpoint. J. Biol. Chem. 277, 27088-27093.
78. Zou, L., Cortez, D., and Elledge, S. J. (2002). Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 16, 198-208.