Caenorhabditis elegans HUS-1 is a DNA damage checkpoint protein required for genome stability and EGL-1-mediated apoptosis

Current Biology

Volumn 12, Issue 22, 2002, Pages 1908-1918

  Hofmann, E Randal ^a,f   Milstein, Stuart ^a,b,c   Boulton, Simon J ^c,d   Ye, Mianjia ^a   Hofmann, Jen J ^a,f   Stergiou, Lilli ^f   Gartner, Anton ^e   Vidal, Marc ^c   Hengartner, Michael O ^a,f  

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

^b STONY BROOK UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^e MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^f UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; CELL CYCLE PROTEIN; EGL 1 PROTEIN, C ELEGANS; EGL-1 PROTEIN, C ELEGANS; GREEN FLUORESCENT PROTEIN; HUS1 PROTEIN, S POMBE; PHOTOPROTEIN; PRIMER DNA; REPRESSOR PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CHEMISTRY; DNA DAMAGE; GENETICS; GENOME; GENOTYPE; HUMAN; MOUSE; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TRANSGENIC ANIMAL;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE PROTEINS; DNA DAMAGE; DNA PRIMERS; GENOME; GENOTYPE; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; MICE; MUTATION; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; CAENORHABDITIS; CAENORHABDITIS ELEGANS; INVERTEBRATA; MAMMALIA; METAZOA;

EID: 0037137445     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0960-9822(02)01262-9     Document Type: Article

References (47)

1. Hoeijmakers, J.H. (2001). Genome maintenance mechanisms for preventing cancer. Nature 411, 366-374.
2. Rich, T., Allen, R.L., and Wyllie, A.H. (2000). Defying death after DNA damage. Nature 407, 777-783.
3. Bach, S.P., Renehan, A.G., and Potten, C.S. (2000). Stem cells: The intestinal stem cell as a paradigm. Carcinogenesis 21, 469-476.
4. Heyer, B.S., MacAuley, A., Behrendtsen, O., and Werb, Z. (2000). Hypersensitivity to DNA damage leads to increased apoptosis during early mouse development. Genes Dev. 14, 2072-2084.
5. Murakami, H., and Nurse, P. (2000). DNA replication and damage checkpoints and meiotic cell cycle controls in the fission and budding yeasts. Biochem. J. 349, 1-12.
6. Bentley, N.J., Holtzman, D.A., Flaggs, G., Keegan, K.S., DeMaggio, A., Ford, J.C., Hoekstra, M., and Carr, A.M. (1996). The Schizosaccharomyces pombe rad3 checkpoint gene. EMBO J. 15, 6641-6651.
7. Horvitz, H.R. (1999). Genetic control of programmed cell death in the nematode Caenorhabditis elegans. Cancer Res. 59, 1701s-1706s.
8. Gumienny, T.L., Lambie, E., Hartwieg, E., Horvitz, H.R., and Hengartner, M.O. (1999). Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126, 1011-1022.
9. Gartner, A., Milstein, S., Ahmed, S., Hodgkin, J., and Hengartner, M.O. (2000). A conserved checkpoint pathway mediates DNA damage-induced apoptosis and cell cycle arrest in C. elegans. Mol. Cell 5, 435-443.
10. Hofmann, E.R., Milstein, S., and Hengartner, M.O. (2000). DNA damage-induced checkpoint pathways in the nematode Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 65, 467-473.
11. Ahmed, S., Alpi, A., Hengartner, M.O., and Gartner, A. (2001). C. elegans RAD-5/CLK-2 defines a new DNA damage checkpoint protein. Curr. Biol. 11, 1934-1944.
12. Derry, W.B., Putzke, A.P., and Rothman, J.H. (2001). Caenorhabditis elegans p53: Role in apoptosis, meiosis, and stress resistance. Science 294, 591-595.
13. Schumacher, B., Hofmann, K., Boulton, S., and Gartner, A. (2001). The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis. Curr. Biol. 11, 1722-1727.
14. Venclovas, C., and Thelen, M.P. (2000). Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes. Nucleic Acids Res. 28, 2481-2493.
15. Boulton, S.J., Gartner, A., Reboul, J., Vaglio, P., Dyson, N., Hill, D.E., and Vidal, M. (2002). Combined functional genomic maps of the C. elegans DNA damage response. Science 295, 127-131.
16. Caspari, T., Dahlen, M., Kanter-Smoler, G., Lindsay, H.D., Hofmann, K., Papadimitriou, K., Sunnerhagen, P., and Carr, A.M. (2000). Characterization of Schizosaccharomyces pombe Hus1: A PCNA-related protein that associates with Rad1 and Rad9. Mol. Cell. Biol. 20, 1254-1262.
17. Kaur, R., Kostrub, C.F., and Enoch, T. (2001). Structure-function analysis of fission yeast Hus1-Rad1-Rad9 checkpoint complex. Mol. Biol. Cell 12, 3744-3758.
18. 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.
19. Takanami, T., Mori, A., Takahashi, H., and Higashitani, A. (2000). Hyper-resistance of meiotic cells to radiation due to a strong expression of a single recA-like gene in Caenorhabditis elegans. Nucleic Acids Res. 28, 4232-4236.
20. Hodgkin, J., Horvitz, H.R., and Brenner, S. (1979). Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91, 67-94.
21. Chin, G.M., and Villeneuve, A.M. (2001). C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G(2) DNA damage checkpoint. Genes Dev. 15, 522-534.
22. Ahmed, S., and Hodgkin, J. (2000). MRT-2 checkpoint protein is required for germline immortality and telomere replication in C. elegans. Nature 403, 159-164.
23. Myung, K., Datta, A., and Kolodner, R.D. (2001). Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell 104, 397-408.
24. Myung, K., Chen, C., and Kolodner, R.D. (2001). Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature 411, 1073-1076.
25. De Stasio, E., Lephoto, C., Azuma, L., Hoist, C., Stanislaus, D., and Uttam, J. (1997). Characterization of revertants of unc-93(e1500) in Caenorhabditis elegans induced by N-ethyl-N-nitrosourea. Genetics 147, 597-608.
26. Conradt, B., and Horvitz, H.R. (1999). The TRA-1A sex determination protein of C. elegans regulates sexually dimorphic cell deaths by repressing the egl-1 cell death activator gene. Cell 98, 317-327.
27. Feng, H., Zhong, W., Punkosdy, G., Gu, S., Zhou, L., Seabolt, E.K., and Kipreos, E.T. (1999). CUL-2 is required for the G1-to-S-phase transition and mitotic chromosome condensation in Caenorhabditis elegans. Nat. Cell Biol. 1, 486-492.
28. Hong, Y., Roy, R., and Ambros, V. (1998). Developmental regulation of a cyclin-dependent kinase inhibitor controls postembryonic cell cycle progression in Caenorhabditis elegans. Development 125, 3585-3597.
29. Bunz, F., Dutriaux, A., Lengauer, C., Waldman, T., Zhou, S., Brown, J.P., Sedivy, J.M., Kinzler, K.W., and Vogelstein, B. (1998). Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282, 1497-1501.
30. 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.
31. Dahlen, M., Olsson, T., Kanter-Smoler, G., Ramne, A., and Sunnerhagen, P. (1998). Regulation of telomere length by check-point genes in Schizosaccharomyces pombe. Mol. Biol. Cell 9, 611-621.
32. Ollmann, M., Young, L.M., Di Como, C.J., Karim, F., Belvin, M., Robertson, S., Whittaker, K., Demsky, M., Fisher, W.W., Buchman, A., et al. (2000). Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell 101, 91-101.
33. Boxem, M., Srinivasan, D.G., and van den Heuvel, S. (1999). The Caenorhabditis elegans gene ncc-1 encodes a cdc2-related kinase required for M phase in meiotic and mitotic cell divisions, but not for S phase. Development 126, 2227-2239.
34. Ashcroft, N., and Golden, A. (2002). CDC-25.1 regulates germline proliferation in Caenorhabditis elegans. Genesis 33, 1-7.
35. Miyashita, T., and Reed, J.C. (1995). Tumor suppressor p53 is a direct transcriptional activator of the human Bax gene. Cell 80, 293-299.
36. Oda, E., Ohki, R., Murasawa, H., Nemoto, J., Shibue, T., Yamashita, T., Tokino, T., Taniguchi, T., and Tanaka, N. (2000). Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288, 1053-1058.
37. Nakano, K., and Vousden, K.H. (2001). PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell 7, 683-694.
38. Yu, J., Zhang, L., Hwang, P.M., Kinzler, K.W., and Vogeistein, B. (2001). PUMA induces the rapid apoptosis of colorectal cancer cells. Mol. Cell 7, 673-682.
39. Barlow, C., Brown, K.D., Deng, C.X., Tagle, D.A., and Wynshaw-Boris, A. (1997). Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways. Nat. Genet. 17, 453-456.
40. 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.
41. Herzog, K.H., Chong, M.J., Kapsetaki, M., Morgan, J.I., and McKinnon, P.J. (1998). Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science 280, 1089-1091.
42. Symonds, H., Krall, L., Remington, L., Saenz-Robles, M., Lowe, S., Jacks, T., and Van Dyke, T. (1994). p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell 78, 703-711.
43. Liu, Q., Guntuku, S., Cui, X.S., Matsuoka, S., Cortez, D., Tamai, K., Luo, G., Carattini-Rivera, S., DeMayo, F., Bradley, A., et al. (2000). Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev. 14, 1448-1459.
44. Brown, E.J., and Baltimore, D. (2000). ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14, 397-402.
45. Jansen, G., Hazendonk, E., Thijssen, K.L., and Plasterk, R.H. (1997). Reverse genetics by chemical mutagenesis in Caenorhabditis elegans. Nat. Genet. 17, 119-121.
46. Praitis, V., Casey, E., Collar, D., and Austin, J. (2001). Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157, 1217-1226.
47. Greenwald, I.S., and Horvitz, H.R. (1980). unc-93(e1500): A behavioral mutant of Caenorhabditis elegans that defines a gene with a wild-type null phenotype. Genetics 96, 147-164.