LEDGF (p75) promotes DNA-end resection and homologous recombination

Nature Structural and Molecular Biology

Volumn 19, Issue 8, 2012, Pages 803-810

  Daugaard, Mads ^a,b   Baude, Annika ^a   Fugger, Kasper ^c   Povlsen, Lou Klitgaard ^a,e   Beck, Halfdan ^c   Sørensen, Claus Storgaard ^c   Petersen, Nikolaj H T ^a   Sorensen, Poul H B ^b   Lukas, Claudia ^a   Bartek, Jiri ^a,d   Lukas, Jiri ^a   Rohde, Mikkel ^a   Jäättelä, Marja ^a  

^a DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d PALACKÝ UNIVERSITY   (Czech Republic)

^e University of Copenhagen   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

LENS EPITHELIUM DERIVED GROWTH FACTOR; PROTEIN P75;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN; DNA REPAIR; DNA STRAND BREAKAGE; EPIGENETICS; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; APOPTOSIS; CARRIER PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; CHROMATIN; DNA BREAKS, DOUBLE-STRANDED; HELA CELLS; HIV; HUMANS; NUCLEAR PROTEINS; RECOMBINATIONAL DNA REPAIR; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; VIRUS INTEGRATION;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84864649532     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2314     Document Type: Article

References (59)

1. Daugaard, M. et al. Lens epithelium-derived growth factor is an Hsp70-2 regulated guardian of lysosomal stability in human cancer. Cancer Res. 67, 2559-2567 (2007).
2. Llano, M. et al. Identifcation and characterization of the chromatin-binding domains of the HIV-1 integrase interactor LEDGF/p75. J. Mol. Biol. 360, 760-773 (2006).
3. Ge, H., Si, Y. & Wolffe, A.P. A novel transcriptional coactivator, p52, functionally interacts with the essential splicing factor ASF/SF2. Mol. Cell 2, 751-759 (1998).
4. Brown-Bryan, T.A. et al. Alternative splicing and caspase-mediated cleavage generate antagonistic variants of the stress oncoprotein LEDGF/p75. Mol. Cancer Res. 6, 1293-1307 (2008).
5. Nishizawa, Y., Usukura, J., Singh, D.P., Chylack, L.T. Jr. & Shinohara, T. Spatial and temporal dynamics of two alternatively spliced regulatory factors, lens epithelium-derived growth factor (ledgf/p75) and p52, in the nucleus. Cell Tissue Res. 305, 107-114 (2001).
6. Dietz, F. et al. The family of hepatoma-derived growth factor proteins: characterization of a new member HRP-4 and classifcation of its subfamilies. Biochem. J. 366, 491-500 (2002).
7. Sutherland, H.G. et al. Disruption of ledgf/psip1 results in perinatal mortality and homeotic skeletal transformations. Mol. Cell. Biol. 26, 7201-7210 (2006).
8. Bartholomeeusen, K. et al. Lens epithelium derived growth factor/p75 interacts with the transposase derived DDE domain of pogZ. J. Biol. Chem. 284, 11467-11477 (2009).
9. Hughes, S., Jenkins, V., Dar, M.J., Engelman, A. & Cherepanov, P. Transcriptional co-activator LEDGF interacts with Cdc7-activator of S-phase kinase (ASK) and stimulates its enzymatic activity. J. Biol. Chem. 285, 541-554 (2010).
10. Maertens, G.N., Cherepanov, P. & Engelman, A. Transcriptional co-activator p75 binds and tethers the Myc-interacting protein JPO2 to chromatin. J. Cell Sci. 119, 2563-2571 (2006).
11. Yokoyama, A. & Cleary, M.L. Menin critically links MLL proteins with LEDGF on cancer-associated target genes. Cancer Cell 14, 36-46 (2008).
12. Ciuff, A. et al. A role for LEDGF/p75 in targeting HIV DNA integration. Nat. Med. 11, 1287-1289 (2005).
13. Shun, M.C. et al. Identifcation and characterization of PWWP domain residues critical for LEDGF/p75 chromatin binding and human immunodefciency virus type 1 infectivity. J. Virol. 82, 11555-11567 (2008).
14. Ciuff, A. Mechanisms governing lentivirus integration site selection. Curr. Gene Ther. 8, 419-429 (2008).
15. De Rijck, J., Bartholomeeusen, K., Ceulemans, H., Debyser, Z. & Gijsbers, R. High-resolution profling of the LEDGF/p75 chromatin interaction in the ENCODE region. Nucleic Acids Res. 38, 6135-6147 (2010).
16. De Luca, L. et al. Small molecules targeting the interaction between HIV-1 integrase and LEDGF/p75 cofactor. Bioorg. Med. Chem. 18, 7515-7521 (2010).
17. Vets, S. et al. Lens epithelium-derived growth factor/p75 qualifes as a target for HIV gene therapy in the NSG mouse model. Mol. Ther. 20, 908-917 (2012).
18. De Luca, L., Ferro, S., Morreale, F. & Chimirri, A. Inhibition of the interaction between HIV-1 integrase and its cofactor LEDGF/p75: a promising approach in anti-retroviral therapy. Mini Rev. Med. Chem. 11, 714-727 (2011).
19. Hussey, D.J., Moore, S., Nicola, M. & Dobrovic, A. Fusion of the NUP98 gene with the LEDGF/p52 gene defnes a recurrent acute myeloid leukemia translocation. BMC Genet. 2, 20 (2001).
20. Daniels, T. et al. Antinuclear autoantibodies in prostate cancer: immunity to LEDGF/p75, a survival protein highly expressed in prostate tumors and cleaved during apoptosis. Prostate 62, 14-26 (2005).
21. Matsui, H., Lin, L.R., Singh, D.P., Shinohara, T. & Reddy, V.N. Lens epithelium-derived growth factor: increased survival and decreased DNA breakage of human RPE cells induced by oxidative stress. Invest. Ophthalmol. Vis. Sci. 42, 2935-2941 (2001).
22. Wang, Y. et al. Regulation of Set9-mediated H4K20 methylation by a PWWP domain protein. Mol. Cell 33, 428-437 (2009).
23. Laguri, C. et al. Human mismatch repair protein MSH6 contains a PWWP domain that targets double stranded DNA. Biochemistry 47, 6199-6207 (2008).
24. Huen, M.S. et al. Regulation of chromatin architecture by the PWWP domain-containing DNA damage-responsive factor EXPAND1/MUM1. Mol. Cell 37, 854-864 (2010).
25. Kousholt, A.N. et al. CtIP-dependent DNA resection is required for DNA damage checkpoint maintenance but not initiation. J. Cell Biol. (in the press).
26. Moynahan, M.E., Cui, T.Y. & Jasin, M. Homology-directed DNA repair, mitomycin-c resistance, and chromosome stability is restored with correction of a Brca1 mutation. Cancer Res. 61, 4842-4850 (2001).
27. Sartori, A.A. et al. Human CtIP promotes DNA end resection. Nature 450, 509-514 (2007).
28. Spencer, D.M. et al. DNA repair in response to anthracycline-DNA adducts: a role for both homologous recombination and nucleotide excision repair. Mutat. Res. 638, 110-121 (2008).
29. Caldecott, K.W. Single-strand break repair and genetic disease. Nat. Rev. Genet. 9, 619-631 (2008).
30. Jackson, S.P. & Bartek, J. The DNA-damage response in human biology and disease. Nature 461, 1071-1078 (2009).
31. Farmer, H. et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434, 917-921 (2005).
32. Bryant, H.E. et al. Specifc killing of BRCA2-defcient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434, 913-917 (2005).
33. Pierce, A.J., Hu, P., Han, M., Ellis, N. & Jasin, M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15, 3237-3242 (2001).
34. Huertas, P. DNA resection in eukaryotes: deciding how to fx the break. Nat. Struct. Mol. Biol. 17, 11-16 (2010).
35. Garcia, V., Phelps, S.E.L., Gray, S. & Neale, M.J. Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1. Nature 479, 241-244 (2011).
36. Bernstein, K.A. & Rothstein, R. At loose ends: resecting a double-strand break. Cell 137, 807-810 (2009).
37. Bekker-Jensen, S. et al. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173, 195-206 (2006).
38. Shao, R.G. et al. Replication-mediated DNA damage by camptothecin induces phosphorylation of RPA by DNA-dependent protein kinase and dissociates RPA: DNA-PK complexes. EMBO J. 18, 1397-1406 (1999).
39. Manthey, K.C. et al. NBS1 mediates ATR-dependent RPA hyperphosphorylation following replication-fork stall and collapse. J. Cell Sci. 120, 4221-4229 (2007).
40. You, Z. et al. CtIP links DNA double-strand break sensing to resection. Mol. Cell 36, 954-969 (2009).
41. Lukas, C., Falck, J., Bartkova, J., Bartek, J. & Lukas, J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 5, 255-260 (2003).
42. Cherepanov, P. et al. Solution structure of the HIV-1 integrase-binding domain in LEDGF/p75. Nat. Struct. Mol. Biol. 12, 526-532 (2005).
43. Vezzoli, A. et al. Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat. Struct. Mol. Biol. 17, 617-619 (2010).
44. Dhayalan, A. et al. The DNMT3A PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation. J. Biol. Chem. 285, 26114-26120 (2010).
45. Saunders, A., Core, L.J. & Lis, J.T. Breaking barriers to transcription elongation. Nat. Rev. Mol. Cell Biol. 7, 557-567 (2006).
46. Liu, F. & Lee, W.H. CtIP activates its own and cyclin D1 promoters via the E2F/RB pathway during G1/S progression. Mol. Cell. Biol. 26, 3124-3134 (2006).
47. Bennardo, N., Cheng, A., Huang, N. & Stark, J.M. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 4, e1000110 (2008).
48. Chen, P.L. et al. Inactivation of CtIP leads to early embryonic lethality mediated by G1 restraint and to tumorigenesis by haploid insuffciency. Mol. Cell. Biol. 25, 3535-3542 (2005).
49. Lim, D.S. & Hasty, P. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16, 7133-7143 (1996).
50. Wang, Y. et al. Mutation in Rpa1 results in defective DNA double-strand break repair, chromosomal instability and cancer in mice. Nat. Genet. 37, 750-755 (2005).
51. Vermeulen, M. et al. Quantitative interaction proteomics and genome-wide profling of epigenetic histone marks and their readers. Cell 142, 967-980 (2010).
52. Skalka, A.M. & Katz, R.A. Retroviral DNA integration and the DNA damage response. Cell Death Differ. 12 (suppl. 1), 971-978 (2005).
53. Katz, R.A., Greger, J.G. & Skalka, A.M. Effects of cell cycle status on early events in retroviral replication. J. Cell. Biochem. 94, 880-889 (2005).
54. Sinclair, A., Yarranton, S. & Schelcher, C. DNA-damage response pathways triggered by viral replication. Expert Rev. Mol. Med. 8, 1-11 (2006).
55. Pommier, Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer 6, 789-802 (2006).
56. Llorente, B., Smith, C.E. & Symington, L.S. Break-induced replication: what is it and what is it for? Cell Cycle 7, 859-864 (2008).
57. Lukas, C., Falck, J., Bartkova, J., Bartek, J. & Lukas, J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 5, 255-260 (2003).
58. Beck, H. et al. Regulators of cyclin-dependent kinases are crucial for maintaining genome integrity in S phase. J. Cell Biol. 188, 629-638 (2010).
59. Huang, W., Sherman, B.T. & Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).