Should I stay or should I go: VCP/p97-mediated chromatin extraction in the DNA damage response

Experimental Cell Research

Volumn 329, Issue 1, 2014, Pages 9-17

  Dantuma, Nico P ^a   Acs, Klara ^a   Luijsterburg, Martijn S ^b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cdc48; DNA damage response; DNA repair; Proteasome; Protein degradation; Ubiquitin; Valosin containing protein VCP

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DOUBLE STRANDED DNA; PROTEASOME; PROTEIN P97; UBIQUITIN; VALOSIN CONTAINING PROTEIN; CDC48 PROTEIN; CELL CYCLE PROTEIN; CHROMATIN;

CHROMATIN; DNA DAMAGE; DNA REPAIR; EXCISION REPAIR; EXTRACT; GENOME; HUMAN; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; REVIEW; ANIMAL; CHROMOSOME STRUCTURE; METABOLISM;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELL CYCLE PROTEINS; CHROMATIN; CHROMOSOME STRUCTURES; DNA DAMAGE; DNA REPAIR; HUMANS; UBIQUITIN;

EID: 84919385184     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.08.025     Document Type: Review

References (61)

1. Bekker-Jensen S., Mailand N. The ubiquitin- and SUMO-dependent signaling response to DNA double-strand breaks. FEBS Lett. 2011, 585(18):2914-2919.
2. Stolz A., et al. Cdc48: a power machine in protein degradation. Trends Biochem. Sci. 2011, 36(10):515-523.
3. Jentsch S., Rumpf S. Cdc48 (p97): a "molecular gearbox" in the ubiquitin pathway?. Trends Biochem. Sci. 2007, 32(1):6-11.
4. Finley D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 2009, 78:477-513.
5. Meyer H., Bug M., Bremer S. Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system. Nat. Cell Biol. 2012, 14(2):117-123.
6. Ramadan K., et al. Cdc48/p97 promotes reformation of the nucleus by extracting the kinase Aurora B from chromatin. Nature 2007, 450(7173):1258-1262.
7. Dantuma N.P., Hoppe T. Growing sphere of influence: Cdc48/p97 orchestrates ubiquitin-dependent extraction from chromatin. Trends Cell Biol. 2012, 22(9):483-491.
8. Meusser B., et al. ERAD: the long road to destruction. Nat. Cell Biol. 2005, 7(8):766-772.
9. de Laat W.L., Jaspers N.G., Hoeijmakers J.H. Molecular mechanism of nucleotide excision repair. Genes Dev. 1999, 13(7):768-785.
10. Wilson M.D., Harreman M., Svejstrup J.Q. Ubiquitylation and degradation of elongating RNA polymerase II: the last resort. Biochim. Biophys. Acta 2013, 1829(1):151-157.
11. Harreman M., et al. Distinct ubiquitin ligases act sequentially for RNA polymerase II polyubiquitylation. Proc. Natl. Acad. Sci. USA 2009, 106(49):20705-20710.
12. Anindya R., Aygun O., Svejstrup J.Q. Damage-induced ubiquitylation of human RNA polymerase II by the ubiquitin ligase Nedd4, but not Cockayne syndrome proteins or BRCA1. Mol. Cell 2007, 28(3):386-397.
13. Verma R., et al. Cdc48/p97 mediates UV-dependent turnover of RNA Pol II. Mol. Cell 2011, 41(1):82-92.
14. Kee Y., Lyon N., Huibregtse J.M. The Rsp5 ubiquitin ligase is coupled to and antagonized by the Ubp2 deubiquitinating enzyme. EMBO J. 2005, 24(13):2414-2424.
15. Nathan J.A., et al. Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes?. EMBO J. 2013, 32(4):552-565.
16. Puumalainen M.R., et al. Chromatin retention of DNA damage sensors DDB2 and XPC through loss of p97 segregase causes genotoxicity. Nat. Commun. 2014, 5:3695.
17. Hoogstraten D., et al. Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC. J. Cell Sci. 2008, 121(Pt 17):2850-2859.
18. Luijsterburg M.S., et al. Dynamic in vivo interaction of DDB2 E3 ubiquitin ligase with UV-damaged DNA is independent of damage-recognition protein XPC. J. Cell Sci. 2007, 120(Pt 15):2706-2716.
19. Scrima A., et al. Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 2008, 135(7):1213-1223.
20. Sugasawa K., et al. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 2005, 121(3):387-400.
21. den Besten W., et al. NEDD8 links cullin-RING ubiquitin ligase function to the p97 pathway. Nat. Struct. Mol. Biol. 2012, 19(5):511-516.
22. Bandau S., et al. UBXN7 docks on neddylated cullin complexes using its UIM motif and causes HIF1alpha accumulation. BMC Biol. 2012, 10:36.
23. Essers J., et al. Nuclear dynamics of PCNA in DNA replication and repair. Mol. Cell. Biol. 2005, 25(21):9350-9359.
24. Arias E.E., Walter J.C. PCNA functions as a molecular platform to trigger Cdt1 destruction and prevent re-replication. Nat. Cell Biol. 2006, 8(1):84-90.
25. Nishitani H., et al. Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J. 2006, 25(5):1126-1136.
26. Raman M., et al. A genome-wide screen identifies p97 as an essential regulator of DNA damage-dependent CDT1 destruction. Mol. Cell 2011, 44(1):72-84.
27. Franz A., et al. CDC-48/p97 coordinates CDT-1 degradation with GINS chromatin dissociation to ensure faithful DNA replication. Mol. Cell 2011, 44(1):85-96.
28. Lehmann A.R., et al. Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair 2007, 6(7):891-899.
29. Bienko M., et al. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 2005, 310(5755):1821-1824.
30. Davis E.J., et al. DVC1 (C1orf124) recruits the p97 protein segregase to sites of DNA damage. Nat. Struct. Mol. Biol. 2012, 19(11):1093-1100.
31. Mosbech A., et al. DVC1 (C1orf124) is a DNA damage-targeting p97 adaptor that promotes ubiquitin-dependent responses to replication blocks. Nat. Struct. Mol. Biol. 2012, 19(11):1084-1092.
32. Centore R.C., et al. Spartan/C1orf124, a reader of PCNA ubiquitylation and a regulator of UV-induced DNA damage response. Mol. Cell 2012, 46(5):625-635.
33. Hofmann K. Ubiquitin-binding domains and their role in the DNA damage response. DNA Repair 2009, 8(4):544-556.
34. Luijsterburg M.S., van Attikum H. Close encounters of the RNF8th kind: when chromatin meets DNA repair. Curr. Opin. Cell Biol. 2012, 24(3):439-447.
35. Huen M.S., et al. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 2007, 131(5):901-914.
36. Mailand N., et al. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 2007, 131(5):887-900.
37. Mattiroli F., et al. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 2012, 150(6):1182-1195.
38. Marteijn J.A., et al. Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response. J. Cell Biol. 2009, 186(6):835-847.
39. Ramadan K., Meerang M. Degradation-linked ubiquitin signal and proteasome are integral components of DNA double strand break repair: new perspectives for anti-cancer therapy. FEBS Lett. 2011, 585(18):2868-2875.
40. Lok G.T., et al. Differential regulation of RNF8-mediated Lys48- and Lys63-based poly-ubiquitylation. Nucleic Acids Res. 2012, 40(1):196-205.
41. Galanty Y., et al. RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev. 2012, 26(11):1179-1195.
42. Feng L., Chen J. The E3 ligase RNF8 regulates KU80 removal and NHEJ repair. Nat. Struct. Mol. Biol. 2012, 19(2):201-206.
43. Meerang M., et al. The ubiquitin-selective segregase VCP/p97 orchestrates the response to DNA double-strand breaks. Nat. Cell Biol. 2011, 13(11):1376-1382.
44. Acs K., et al. The AAA-ATPase VCP/p97 promotes 53BP1 recruitment by removing L3MBTL1 from DNA double-strand breaks. Nat. Struct. Mol. Biol. 2011, 18(12):1345-1350.
45. Ye Y., Meyer H.H., Rapoport T.A. Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J. Cell Biol. 2003, 162(1):71-84.
46. Dantuma N.P., et al. A dynamic ubiquitin equilibrium couples proteasomal activity to chromatin remodeling. J. Cell Biol. 2006, 173(1):19-26.
47. Panier S., Boulton S.J. Double-strand break repair: 53BP1 comes into focus. Nat. Rev. Mol. Cell Biol. 2014, 15(1):7-18.
48. Min J., et al. L3MBTL1 recognition of mono- and dimethylated histones. Nat. Struct. Mol. Biol. 2007, 14(12):1229-1230.
49. Kato K., et al. Fine-tuning of DNA damage-dependent ubiquitination by OTUB2 supports the DNA repair pathway choice. Mol. Cell 2014, 53(4):617-630.
50. Mallette F.A., et al. RNF8- and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J. 2012, 31(8):1865-1878.
51. Fradet-Turcotte A., et al. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 2013, 499(7456):50-54.
52. Bergink S., et al. Role of Cdc48/p97 as a SUMO-targeted segregase curbing Rad51-Rad52 interaction. Nat. Cell Biol. 2013, 15(5):526-532.
53. Yang H., et al. The BRCA2 homologue Brh2 nucleates RAD51 filament formation at a dsDNA-ssDNA junction. Nature 2005, 433(7026):653-657.
54. Ju J.S., et al. Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease. J. Cell Biol. 2009, 187(6):875-888.
55. Tresse E., et al. VCP/p97 is essential for maturation of ubiquitin-containing autophagosomes and this function is impaired by mutations that cause IBMPFD. Autophagy 2010, 6(2):217-227.
56. Buchan J.R., et al. Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell 2013, 153(7):1461-1474.
57. Johnson J.O., et al. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 2010, 68(5):857-864.
58. Watts G.D., et al. Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat. Genet. 2004, 36(4):377-381.
59. La Spada A.R., Taylor J.P. Repeat expansion disease: progress and puzzles in disease pathogenesis. Nat. Rev. Genet. 2010, 11(4):247-258.
60. McKinnon P.J. DNA repair deficiency and neurological disease. Nat. Rev. Neurosci. 2009, 10(2):100-112.
61. Fujita K., et al. A functional deficiency of TERA/VCP/p97 contributes to impaired DNA repair in multiple polyglutamine diseases. Nat. Commun. 2013, 4:1816.