The role of the human psoralen 4 (hPso4) protein complex in replication stress and homologous recombination

Journal of Biological Chemistry

Volumn 289, Issue 20, 2014, Pages 14009-14019

  Abbas, Mohammad ^a   Shanmugam, Ilanchezhian ^a   Bsaili, Manal ^a   Hromas, Robert ^b   Shaheen, Monte ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; PROTEINS; REPAIR;

CONSERVED PROTEINS; DNA DOUBLE STRAND BREAKS; DNA REPLICATIONS; GENOME STABILITY; HOMOLOGOUS RECOMBINATION; INTERSTRAND CROSS-LINKS; PROTEIN COMPLEXES; SINGLE STRAND DNA;

DNA;

BRCA1 PROTEIN; HUMAN PSORALEN 4 COMPLEX; HYDROXYUREA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PSORALEN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; CYCLINE; ENZYME INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NUCLEAR PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PRPF19 PROTEIN, HUMAN;

ARTICLE; CANCER CELL; CELL CYCLE S PHASE; CELL PROLIFERATION; CONTROLLED STUDY; DNA CROSS LINKING; DNA DAMAGE; DNA REPAIR; DNA STRAND; DNA STRAND BREAKAGE; DOUBLE STRANDED DNA BREAK; G2 PHASE CELL CYCLE CHECKPOINT; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SENSITIVITY ANALYSIS; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; DEFICIENCY; DNA REPLICATION; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; PROTEIN TRANSPORT; RADIATION RESPONSE;

BRCA1 PROTEIN; CELL LINE; CELL PROLIFERATION; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPAIR ENZYMES; DNA REPLICATION; DNA, SINGLE-STRANDED; ENZYME INHIBITORS; HOMOLOGOUS RECOMBINATION; HUMANS; HYDROXYUREA; NUCLEAR PROTEINS; POLY(ADP-RIBOSE) POLYMERASES; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN TRANSPORT;

EID: 84901044867     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.520056     Document Type: Article

References (43)

1. Brendel, M., and Henriques, J. A. (2001) The Pso mutants of Saccharomyces cerevisiae comprise two groups: one deficient in DNA repair and another with altered mutagen metabolism. Mutat. Res. 489, 79-96
2. Grey, M., Düsterhöft, A., Henriques, J. A., and Brendel, M. (1996) Allelism of PSO4 and PRP19 links pre-mRNA processing with recombination and error-prone DNA repair in Saccharomyces cerevisiae. Nucleic Acids Res. 24, 4009-4014
3. Ohi, M. D., Vander Kooi, C. W., Rosenberg, J. A., Chazin, W. J., and Gould, K. L. (2003) Structural insights into the U-box, a domain associated with multi-ubiquitination. Nat. Struct. Biol. 10, 250-255
4. Hatakeyama, S., Yada, M., Matsumoto, M., Ishida, N., and Nakayama, K. I. (2001) U box proteins as a new family of ubiquitin-protein ligases. J. Biol. Chem. 276, 33111-33120
5. Grote, M., Wolf, E., Will, C. L., Lemm, I., Agafonov, D. E., Schomburg, A., Fischle, W., Urlaub, H., and Lührmann, R. (2010) Molecular architecture of the human Prp19/CDC5L complex. Mol. Cell. Biol. 30, 2105-2119
6. Chan, S. P., Kao, D. I., Tsai, W. Y., and Cheng, S. C. (2003) The Prp19passociated complex in spliceosome activation. Science 302, 279-282
7. Zhang, N., Kaur, R., Lu, X., Shen, X., Li, L., and Legerski, R. J. (2005) The Pso4 mRNA splicing and DNA repair complex interacts with WRN for processing of DNA interstrand cross-links. J. Biol. Chem. 280, 40559-40567
8. Zhang, N., Kaur, R., Akhter, S., and Legerski, R. J. (2009) Cdc5L interacts with ATR and is required for the S-phase cell-cycle checkpoint. EMBO Rep. 10, 1029-1035
9. Deans, A. J., and West, S. C. (2011) DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer 11, 467-480
10. Petermann, E., Orta, M. L., Issaeva, N., Schultz, N., and Helleday, T. (2010) Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 37, 492-502
11. Hanada, K., Budzowska, M., Davies, S. L., van Drunen, E., Onizawa, H., Beverloo, H. B., Maas, A., Essers, J., Hickson, I. D., and Kanaar, R. (2007) The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struct. Mol. Biol. 14, 1096-1104
12. Sedelnikova, O. A., Pilch, D. R., Redon, C., and Bonner, W. M. (2003) Histone H2AX in DNA damage and repair. Cancer Biol. Ther. 2, 233-235
13. Petermann, E., and Helleday, T. (2010) Pathways of mammalian replication fork restart. Nat. Rev. Mol. Cell. Biol. 11, 683-687
14. Pierce, A. J., Johnson, R. D., Thompson, L. H., and Jasin, M. (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 13, 2633-2638
15. Vander Kooi, C. W., Ohi, M. D., Rosenberg, J. A., Oldham, M. L., Newcomer, M. E., Gould, K. L., and Chazin, W. J. (2006) The Prp19 U-box crystal structure suggests a common dimeric architecture for a class of oligomeric E3 ubiquitin ligases. Biochemistry 45, 121-130
16. Groth, P., Orta, M. L., Elvers, I., Majumder, M. M., Lagerqvist, A., and Helleday, T. (2012) Homologous recombination repairs secondary replication induced DNA double-strand breaks after ionizing radiation. Nucleic Acids Res. 40, 6585-6594
17. Shaheen, M., Allen, C., Nickoloff, J. A., and Hromas, R. (2011) Synthetic lethality: exploiting the addiction of cancer to DNA repair. Blood 117, 6074-6082
18. Llères, D., Denegri, M., Biggiogera, M., Ajuh, P., and Lamond, A. I. (2010) Direct interaction between hnRNP-M and CDC5L/PLRG1 proteins affects alternative splice site choice. EMBO Rep. 11, 445-451
19. Wang, B., Hurov, K., Hofmann, K., and Elledge, S. J. (2009) NBA1, a new player in the BRCA1-A complex, is required for DNA damage resistance and checkpoint control. Genes Dev. 23, 729-739
20. Sowa, M. E., Bennett, E. J., Gygi, S. P., and Harper, J. W. (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403
21. Choudhury, A. D., Xu, H., and Baer, R. (2004) Ubiquitination and proteasomal degradation of the BRCA1 tumor suppressor is regulated during cell cycle progression. J. Biol. Chem. 279, 33909-33918
22. Yun, M. H., and Hiom, K. (2009) CtIP-BRCA1 modulates the choice of DNA double-strand break repair pathway throughout the cell cycle. Nature 459, 460-463
23. Fotedar, R., and Roberts, J. M. (1992) Cell cycle regulated phosphorylation of RPA-32 occurs within the replication initiation complex. EMBO J. 11, 2177-2187
24. Feng, Z., and Zhang, J. (2012) A dual role of BRCA1 in two distinct homologous recombination mediated repair in response to replication arrest. Nucleic Acids Res. 40, 726-738
25. Schlegel, B. P., Jodelka, F. M., and Nunez, R. (2006) BRCA1 promotes induction of ssDNA by ionizing radiation. Cancer Res. 66, 5181-5189
26. Kleinridders, A., Pogoda, H. M., Irlenbusch, S., Smyth, N., Koncz, C., Hammerschmidt, M., and Brüning, J. C. (2009) PLRG1 is an essential regulator of cell proliferation and apoptosis during vertebrate development and tissue homeostasis. Mol. Cell. Biol. 29, 3173-3185
27. Fortschegger, K., Wagner, B., Voglauer, R., Katinger, H., Sibilia, M., and Grillari, J. (2007) Early embryonic lethality of mice lacking the essential protein SNEV. Mol. Cell. Biol. 27, 3123-3130
28. Nurse, P., Thuriaux, P., and Nasmyth, K. (1976) Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe. Mol. Gen. Genet. 146, 167-178
29. Lu, X. Y., Lu, Y., Zhao, Y. J., Jaeweon, K., Kang, J., Xiao-Nan, L., Ge, G., Meyer, R., Perlaky, L., Hicks, J., Chintagumpala, M., Cai, W. W., Ladanyi, M., Gorlick, R., Lau, C. C., Pati, D., Sheldon, M., and Rao, P. H. (2008) Cell cycle regulator gene CDC5L, a potential target for 6p12-p21 amplicon in osteosarcoma. Mol. Cancer Res. 6, 937-946
30. Maass, N., Rösel, F., Schem, C., Hitomi, J., Jonat, W., and Nagasaki, K. (2002) Amplification of the BCAS2 gene at chromosome 1p13.3-21 in human primary breast cancer. Cancer Lett. 185, 219-223
31. Bartkova, J., Horejsí, Z., Koed, K., Krämer, A., Tort, F., Zieger, K., Guldberg, P., Sehested, M., Nesland, J. M., Lukas, C., Ørntoft, T., Lukas, J., and Bartek, J. (2005) DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434, 864-870
32. Paulsen, R. D., Soni, D. V., Wollman, R., Hahn, A. T., Yee, M. C., Guan, A., Hesley, J. A., Miller, S. C., Cromwell, E. F., Solow-Cordero, D. E., Meyer, T., and Cimprich, K. A. (2009) A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol. Cell 35, 228-239
33. Budzowska, M., and Kanaar, R. (2009) Mechanisms of dealing with DNA damage-induced replication problems. Cell Biochem. Biophys. 53, 17-31
34. Beck, B. D., Park, S. J., Lee, Y. J., Roman, Y., Hromas, R. A., and Lee, S. H. (2008) Human Pso4 is a metnase (SETMAR)-binding partner that regulates metnase function in DNA repair. J. Biol. Chem. 283, 9023-9030
35. Williams, G. J., Lees-Miller, S. P., and Tainer, J. A. (2010) Mre11-Rad50- Nbs1 conformations and the control of sensing, signaling, and effector responses at DNA double-strand breaks. DNA Repair 9, 1299-1306
36. Yang, E. S., and Xia, F. (2010) BRCA1 16 years later:DNAdamage-induced BRCA1 shuttling. FEBS J. 277, 3079-3085
37. Long, D. T., Räschle, M., Joukov, V., and Walter, J. C. (2011) Mechanism of RAD51-dependent DNA interstrand cross-link repair. Science 333, 84-87
38. Song, E. J., Werner, S. L., Neubauer, J., Stegmeier, F., Aspden, J., Rio, D., Harper, J. W., Elledge, S. J., Kirschner, M. W., and Rape, M. (2010) The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev. 24, 1434-1447
39. Popov, N., Schülein, C., Jaenicke, L. A., and Eilers, M. (2010) Ubiquitylation of the amino terminus of Myc by SCF(β-TrCP) antagonizes SCF(Fbw7)-mediated turnover. Nat. Cell Biol. 12, 973-981
40. Reid, L. J., Shakya, R., Modi, A. P., Lokshin, M., Cheng, J. T., Jasin, M., Baer, R., and Ludwig, T. (2008) E3 ligase activity of BRCA1 is not essential for mammalian cell viability or homology-directed repair of double-strand DNA breaks. Proc. Natl. Acad. Sci. U.S.A. 105, 20876-20881
41. Silver, D. P., and Livingston, D. M. (2012) Mechanisms of BRCA1 tumor suppression. Cancer Discovery 2, 679-684
42. Farmer, H., McCabe, N., Lord, C. J., Tutt, A. N., Johnson, D. A., Richardson, T. B., Santarosa, M., Dillon, K. J., Hickson, I., Knights, C., Martin, N. M., Jackson, S. P., Smith, G. C., and Ashworth, A. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434, 917-921
43. Bryant, H. E., Schultz, N., Thomas, H. D., Parker, K. M., Flower, D., Lopez, E., Kyle, S., Meuth, M., Curtin, N. J., and Helleday, T. (2005) Specific killing of BRCA2-deficient tumors with inhibitors of poly(ADP-ribose) polymerase. Nature 434, 913-917