Depletion of DSS1 protein disables homologous recombinational repair in human cells

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 694, Issue 1-2, 2010, Pages 60-64

  Kristensen, Colleen N ^a   Bystol, Karin M ^a   Li, Boran ^a   Serrano, Lourdes ^a   Brenneman, Mark A ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

Author keywords

BRCA2; DNA repair; DSS1; Homologous recombination; Proteasomes

Indexed keywords

BRCA2 PROTEIN; DELETED IN SPLIT HAND PROTEIN; DEOXYRIBONUCLEOPROTEIN; PROTEASOME; SHORT HAIRPIN RNA; SPLIT FOOT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; COLONY FORMING UNIT; CONTROLLED STUDY; DNA BINDING; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; USTILAGO MAYDIS;

BRCA2 PROTEIN; CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; GENE SILENCING; HUMANS; MODELS, GENETIC; MUTATION; POLYMERASE CHAIN REACTION; PROTEASOME ENDOPEPTIDASE COMPLEX; RECOMBINATION, GENETIC; RNA INTERFERENCE;

EUKARYOTA; MAMMALIA; PROTISTA; USTILAGO MAYDIS;

EID: 78649433314     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2010.08.007     Document Type: Article

References (34)

1. Crackower M.A., Scherer S.W., Rommens J.M., Hui C.C., Poorkaj P., Soder S., Cobben J.M., Hudgins L., Evans J.P., Tsui L.C. Characterization of the split hand/split foot malformation locus SHFM1 at 7q21.3-q22.1 and analysis of a candidate gene for its expression during limb development. Hum. Mol. Genet. 1996, 5:571-579.
2. Marston N.J., Richards W.J., Hughes D., Bertwistle D., Marshall C.J., Ashworth A. Interaction between the product of the breast cancer susceptibility gene BRCA2 and DSS1, a protein functionally conserved from yeast to mammals. Mol. Cell. Biol. 1999, 19:4633-4642.
3. Kojic M., Yang H., Kostrub C.F., Pavletich N.P., Holloman W.K. The BRCA2-interacting protein DSS1 is vital for DNA repair, recombination, and genome stability in Ustilago maydis. Mol. Cell 2003, 12:1043-1049.
4. Sone T., Saeki Y., Toh-e A., Yokosawa H. Sem1p is a novel subunit of the 26S proteasome from Saccharomyces cerevisiae. J. Biol. Chem. 2004, 279:28807-28816.
5. Funakoshi M., Li X., Velichutina I., Hochstrasser M., Kobayashi H. Sem1, the yeast ortholog of a human BRCA2-binding protein, is a component of the proteasome regulatory particle that enhances proteasome stability. J. Cell Sci. 2004, 117:6447-6454.
6. Thakurta A.G., Gopal G., Yoon J.H., Kozak L., Dhar R. Homolog of BRCA2-interacting Dss1p and Uap56p link Mlo3p and Rae1p for mRNA export in fission yeast. EMBO J 2005, 24:2512-2523.
7. Dray E., Siaud N., Dubois E., Doutriaux M.P. Interaction between Arabidopsis Brca2 and its partners Rad51, Dmc1, and Dss1. Plant Physiol. 2006, 140:1059-1069.
8. Pispa J., Palmen S., Holmberg C.I., Jantti J. C. elegans dss-1 is functionally conserved and required for oogenesis and larval growth. BMC Dev. Biol. 2008, 8:51.
9. Krogan N.J., Lam M.H., Fillingham J., Keogh M.C., Gebbia M., Li J., Datta N., Cagney G., Buratowski S., Emili A., Greenblatt J.F. Proteasome involvement in the repair of DNA double-strand breaks. Mol. Cell 2004, 16:1027-1034.
10. Josse L., Harley M.E., Pires I.M., Hughes D.A. Fission yeast Dss1 associates with the proteasome and is required for efficient ubiquitin-dependent proteolysis. Biochem. J. 2006, 393:303-309.
11. Gudmundsdottir K., Lord C.J., Ashworth A. The proteasome is involved in determining differential utilization of double-strand break repair pathways. Oncogene 2007, 26:7601-7606.
12. Jacquemont C., Taniguchi T. Proteasome function is required for DNA damage response and Fanconi anemia pathway activation. Cancer Res. 2007, 67:7395-7405.
13. Wei S.J., Williams J.G., Dang H., Darden T.A., Betz B.L., Humble M.M., Chang F.M., Trempus C.S., Johnson K., Cannon R.E., Tennant R.W. Identification of a specific motif of the DSS1 protein required for proteasome interaction and p53 protein degradation. J. Mol. Biol. 2008, 383:693-712.
14. Wilmes G.M., Bergkessel M., Bandyopadhyay S., Shales M., Braberg H., Cagney G., Collins S.R., Whitworth G.B., Kress T.L., Weissman J.S., Ideker T., Guthrie C., Krogan N.J. A genetic interaction map of RNA-processing factors reveals links between Sem1/Dss1-containing complexes and mRNA export and splicing. Mol. Cell 2008, 32:735-746.
15. Faza M.B., Kemmler S., Jimeno S., Gonzalez-Aguilera C., Aguilera A., Hurt E., Panse V.G. Sem1 is a functional component of the nuclear pore complex-associated messenger RNA export machinery. J. Cell Biol. 2009, 184:833-846.
16. Howlett N.G., Taniguchi T., Olson S., Cox B., Waisfisz Q., De Die-Smulders C., Persky N., Grompe M., Joenje H., Pals G., Ikeda H., Fox E.A., D'Andrea A.D. Biallelic inactivation of BRCA2 in Fanconi anemia. Science 2002, 297:606-609.
17. Shivji M.K., Venkitaraman A.R. DNA recombination, chromosomal stability and carcinogenesis: insights into the role of BRCA2. DNA Repair (Amst) 2004, 3:835-843.
18. Yang H., Li Q., Fan J., Holloman W.K., Pavletich N.P. The BRCA2 homologue Brh2 nucleates RAD51 filament formation at a dsDNA-ssDNA junction. Nature 2005, 433:653-657.
19. San Filippo J., Chi P., Sehorn M.G., Etchin J., Krejci L., Sung P. Recombination mediator and Rad51 targeting activities of a human BRCA2 polypeptide. J. Biol. Chem. 2006, 281:11649-11657.
20. Yang H., Jeffrey P.D., Miller J., Kinnucan E., Sun Y., Thoma N.H., Zheng N., Chen P.L., Lee W.H., Pavletich N.P. BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science 2002, 297:1837-1848.
21. Kojic M., Zhou Q., Lisby M., Holloman W.K. Brh2-Dss1 interplay enables properly controlled recombination in Ustilago maydis. Mol. Cell. Biol. 2005, 25:2547-2557.
22. Zhou Q., Kojic M., Cao Z., Lisby M., Mazloum N.A., Holloman W.K. Dss1 interaction with Brh2 as a regulatory mechanism for recombinational repair. Mol. Cell. Biol. 2007, 27:2512-2526.
23. Zhou Q., Kojic M., Holloman W.K. DNA-binding domain within the Brh2 N terminus is the primary interaction site for association with DNA. J. Biol. Chem. 2009, 284:8265-8273.
24. Gudmundsdottir K., Lord C.J., Witt E., Tutt A.N., Ashworth A. DSS1 is required for RAD51 focus formation and genomic stability in mammalian cells. EMBO Rep. 2004, 5:989-993.
25. Haaf T., Golub E.I., Reddy G., Radding C.M., Ward D.C. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:2298-2302.
26. Pellegrini L., Yu D.S., Lo T., Anand S., Lee M., Blundell T.L., Venkitaraman A.R. Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature 2002, 420:287-293.
27. Li J., Zou C., Bai Y., Wazer D.E., Band V., Gao Q. DSS1 is required for the stability of BRCA2. Oncogene 2006, 25:1186-1194.
28. Kim P.M., Allen C., Wagener B.M., Shen Z., Nickoloff J.A. Overexpression of human RAD51 and RAD52 reduces double-strand break-induced homologous recombination in mammalian cells. Nucleic Acids Res. 2001, 29:4352-4360.
29. Lio Y.C., Schild D., Brenneman M.A., Redpath J.L., Chen D.J. Human Rad51C deficiency destabilizes XRCC3, impairs recombination, and radiosensitizes S/G2-phase cells. J. Biol. Chem. 2004, 279:42313-42320.
30. Murakawa Y., Sonoda E., Barber L.J., Zeng W., Yokomori K., Kimura H., Niimi A., Lehmann A., Zhao G.Y., Hochegger H., Boulton S.J., Takeda S. Inhibitors of the proteasome suppress homologous DNA recombination in mammalian cells. Cancer Res. 2007, 67:8536-8543.
31. Rock K.L., Gramm C., Rothstein L., Clark K., Stein R., Dick L., Hwang D., Goldberg A.L. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 1994, 78:761-771.
32. Kessler B.M., Tortorella D., Altun M., Kisselev A.F., Fiebiger E., Hekking B.G., Ploegh H.L., Overkleeft H.S. Extended peptide-based inhibitors efficiently target the proteasome and reveal overlapping specificities of the catalytic beta-subunits. Chem. Biol. 2001, 8:913-929.
33. Ivanov E.L., Sugawara N., Fishman-Lobell J., Haber J.E. Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics 1996, 142:693-704.
34. Kojic M., Holloman W.K. BRCA2-RAD51-DSS1 interplay examined from a microbial perspective. Cell Cycle 2004, 3:247-248.