Recruitment of phosphorylated NPM1 to sites of DNA damage through RNF8-dependent ubiquitin conjugates

Cancer Research

Volumn 70, Issue 17, 2010, Pages 6746-6756

  Koike, Ayaka ^a   Nishikawa, Hiroyuki ^a   Wu, Wenwen ^a   Okada, Yukinori ^a   Venkitaraman, Ashok R ^b   Ohta, Tomohiko ^a  

^a ST MARIANNA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b HUTCHISON MRC RESEARCH CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; CYCLIN DEPENDENT KINASE 2; DOUBLE STRANDED DNA; NUCLEOPHOSMIN; PROTEIN RAP 80; PROTEIN RNF 168; PROTEIN RNF 8; RAP PROTEIN; SINGLE STRANDED DNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ATP DEPENDENT 26S PROTEASE; BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; BRCA1 PROTEIN, HUMAN; DNA BINDING PROTEIN; LEUPEPTIN; NUCLEAR PROTEIN; PROTEASOME; PROTEASOME INHIBITOR; RNF8 PROTEIN, HUMAN; UBIQUITIN;

ARTICLE; DNA DAMAGE; DNA REPAIR; IONIZING RADIATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SINGLE STRANDED DNA BREAK; DEFICIENCY; DOUBLE STRANDED DNA BREAK; HELA CELL LINE; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

BRCA1 PROTEIN; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; LEUPEPTINS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; UBIQUITIN;

EID: 77956274850     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-0382     Document Type: Article

References (46)

1. Harper JW, Elledge SJ. The DNA damage response: ten years after. Mol Cell 2007;28:739-45.
2. Bassing CH, Suh H, Ferguson DO, et al. Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell 2003;114:359-70.
3. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, et al. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 2003;5:675-9.
4. Mailand N, Bekker-Jensen S, Faustrup H, et al. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 2007;131:887-900.
5. Huen MS, Grant R, Manke I, et al. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 2007;131:901-14.
6. Kolas NK, Chapman JR, Nakada S, et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 2007;318:1637-40.
7. Doil C, Mailand N, Bekker-Jensen S, et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 2009;136:435-46.
8. Stewart GS, Panier S, Townsend K, et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 2009;136:420-34.
9. Wang B, Matsuoka S, Ballif BA, et al. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 2007;316:1194-8.
10. Sobhian B, Shao G, Lilli DR, et al. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 2007;316:1198-202.
11. Kim H, Chen J, Yu X. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 2007;316:1202-5.
12. Zhang F, Ma J, Wu J, et al. PALB2 links BRCA1 and BRCA2 in the DNA-damage response. Curr Biol 2009;19:524-9.
13. Yu VP, Koehler M, Steinlein C, et al. Gross chromosomal rearrangements and genetic exchange between nonhomologous chromosomes following BRCA2 inactivation. Genes Dev 2000;14:1400-6.
14. Sato K, Hayami R, Wu W, et al. Nucleophosmin/B23 is a candidate substrate for the BRCA1-1 ubiquitin ligase. J Biol Chem 2004;279:30919-22.
15. Grisendi S, Mecucci C, Falini B, Pandolfi PP. Nucleophosmin and cancer. Nat Rev Cancer 2006;6:493-505.
16. Morris SW, Kirstein MN, Valentine MB, et al. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma. Science 1994;263:1281-4.
17. Yoneda-Kato N, Kato JY. Shuttling imbalance of MLF1 results in p53 instability and increases susceptibility to oncogenic transformation. Mol Cell Biol 2008;28:422-34.
18. Falini B, Mecucci C, Tiacci E, et al. Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N Engl J Med 2005;352:254-66.
19. Kurki S, Peltonen K, Latonen L, et al. Nucleolar protein NPM interacts with HDM2 and protects tumor suppressor protein p53 from HDM2-mediated degradation. Cancer Cell 2004;5:465-75.
20. Rubbi CP, Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 2003;22:6068-77.
21. Wu MH, Chang JH, Yung BY. Resistance to UV-induced cell-killing in nucleophosmin/B23 over-expressed NIH 3T3 fibroblasts: enhancement of DNA repair and up-regulation of PCNA in association with nucleophosmin/B23 over-expression. Carcinogenesis 2002;23:93-100.
22. Lee SY, Park JH, Kim S, Park EJ, Yun Y, Kwon J. A proteomics approach for the identification of nucleophosmin and heterogeneous nuclear ribonucleoprotein C1/C2 as chromatin-binding proteins in response to DNA double-strand breaks. Biochem J 2005;388:7-15.
23. Nishikawa H, Wu W, Koike A, et al. BRCA1-associated protein 1 interferes with BRCA1/BARD1 RING heterodimer activity. Cancer Res 2009;69:111-9.
24. Wu W, Nishikawa H, Hayami R, et al. BRCA1 ubiquitinates RPB8 in response to DNA damage. Cancer Res 2007;67:951-8.
25. Nishikawa H, Ooka S, Sato K, et al. Mass spectrometric and mutational analyses reveal Lys-6-linked polyubiquitin chains catalyzed by BRCA1-1 ubiquitin ligase. J Biol Chem 2004;279:3916-24.
26. Namboodiri VM, Akey IV, Schmidt-Zachmann MS, Head JF, Akey CW. The structure and function of Xenopus NO38-core, a histone chaperone in the nucleolus. Structure 2004;12:2149-60.
27. Lee HH, Kim HS, Kang JY, et al. Crystal structure of human nucleophosmin-core reveals plasticity of the pentamer-pentamer interface. Proteins 2007;69:672-8.
28. Pinato S, Scandiuzzi C, Arnaudo N, Citterio E, Gaudino G, Penengo L. RNF168, a new RING finger, MIU-containing protein that modifies chromatin by ubiquitination of histones H2A and H2AX. BMC Mol Biol 2009;10:55.
29. Huang J, Huen MS, Kim H, et al. RAD18 transmits DNA damage signalling to elicit homologous recombination repair. Nat Cell Biol 2009;11:592-603.
30. Wang B, Hurov K, Hofmann K, Elledge SJ. NBA1, a new player in the Brca1 A complex, is required for DNA damage resistance and checkpoint control. Genes Dev 2009;23:729-39.
31. Hofmann K, Falquet L. A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem Sci 2001;26:347-50.
32. Fisher RD, Wang B, Alam SL, et al. Structure and ubiquitin binding of the ubiquitin-interacting motif. J Biol Chem 2003;278:28976-84.
33. Swanson KA, Kang RS, Stamenova SD, Hicke L, Radhakrishnan I. Solution structure of Vps27 UIM-ubiquitin complex important for endosomal sorting and receptor downregulation. EMBO J 2003;22:4597-606.
34. Hurley JH, Lee S, Prag G. Ubiquitin-binding domains. Biochem J 2006;399:361-72.
35. Sims JJ, Cohen RE. Linkage-specific avidity defines the lysine 63-linked polyubiquitin-binding preference of rap80. Mol Cell 2009;33:775-83.
36. Sato Y, Yoshikawa A, Mimura H, Yamashita M, Yamagata A, Fukai S. Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by tandem UIMs of RAP80. EMBO J 2009;28:2461-8.
37. Okuda M, Horn HF, Tarapore P, et al. Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication. Cell 2000;103:127-40.
38. Tokuyama Y, Horn HF, Kawamura K, Tarapore P, Fukasawa K. Specific phosphorylation of nucleophosmin on Thr(199) by cyclin-dependent kinase 2-cyclin E and its role in centrosome duplication. J Biol Chem 2001;276:21529-37.
39. Negi SS, Olson MO. Effects of interphase and mitotic phosphorylation on the mobility and location of nucleolar protein B23. J Cell Sci 2006;119:3676-85.
40. Swaminathan V, Kishore AH, Febitha KK, Kundu TK. Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription. Mol Cell Biol 2005;25:7534-45.
41. Okuwaki M, Matsumoto K, Tsujimoto M, Nagata K. Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett 2001;506:272-6.
42. Grisendi S, Bernardi R, Rossi M, et al. Role of nucleophosmin in embryonic development and tumorigenesis. Nature 2005;437:147-53.
43. Colombo E, Bonetti P, Lazzerini Denchi E, et al. Nucleophosmin is required for DNA integrity and p19Arf protein stability. Mol Cell Biol 2005;25:8874-86.
44. Vanderwaal RP, Maggi LBJ, Weber JD, Hunt CR, Roti Roti JL. Nucleophosmin redistribution following heat shock: a role in heat-induced radiosensitization. Cancer Res 2009;69:6454-62.
45. Kuo ML, Bertwistle B, Roussel D, Sherr MF. N-terminal polyubiquitination and degradation of the Art tumor suppressor. Genes Dev 2004;18:1862-74.
46. Chen D, Shan J, Zhu W, Qin J, Gu W. Transcription-independent ARF regulation in oncogenic stress-mediated p53 responses. Nature 2010;464:624-7.