Ionizing radiation induces a dramatic persistence of p53 protein accumulation and DNA damage signaling in mutant p53 zebrafish

Oncogene

Volumn 32, Issue 34, 2013, Pages 4009-4016

  Guo, L ^a   Liew, H P ^a   Camus, S ^a   Goh, A M ^a   Chee, L L ^a   Lunny, D P ^b   Lane, E B ^b   Lane, D P ^a  

^a Biomedical Institutes   (Singapore)

^b INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

DNA damage; Ionizing radiation; Mutant; p53 protein; Stability; Zebrafish

Indexed keywords

HISTONE H2AX; MESSENGER RNA; NUTLIN 3; PROTEIN MDM2; PROTEIN MDMX; PROTEIN P53;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DNA DAMAGE; IMMUNOHISTOCHEMISTRY; IONIZING RADIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RADIATION DOSE; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WILD TYPE; ZEBRA FISH;

ANIMALS; BLOTTING, WESTERN; DNA DAMAGE; EMBRYO, NONMAMMALIAN; EYE NEOPLASMS; GENE KNOCKDOWN TECHNIQUES; HISTONES; IMIDAZOLES; IMMUNOHISTOCHEMISTRY; MUTANT PROTEINS; MUTATION; NEOPLASMS, RADIATION-INDUCED; PHOSPHOPROTEINS; PIPERAZINES; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-MDM2; RADIATION, IONIZING; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO; MUS;

EID: 84883199974     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.409     Document Type: Article

References (39)

1. Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science 1991; 253: 49-53.
2. Iggo R, Gatter K, Bartek J, Lane D, Harris AL. Increased expression of mutant forms of p53 oncogene in primary lung cancer. Lancet 1990; 335: 675-679.
3. Bartek J, Bartkova J, Vojtesek B, Staskova Z, Lukas J, Rejthar A et al. Aberrant expression of the p53 oncoprotein is a common feature of a wide spectrum of human malignancies. Oncogene 1991; 6: 1699-1703.
4. Olive KP, Tuveson DA, Ruhe ZC, Yin B, Willis NA, Bronson RT et al. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004; 119: 847-860.
5. Lang GA, Iwakuma T, Suh YA, Liu G, Rao VA, Parant JM et al. Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome. Cell 2004; 119: 861-872.
6. Song H, Hollstein M, Xu Y. p53 gain-of-function cancer mutants induce genetic instability by inactivating ATM. Nat Cell Biol 2007; 9: 573-580.
7. Terzian T, Suh YA, Iwakuma T, Post SM, Neumann M, Lang GA et al. The inherent instability of mutant p53 is alleviated by Mdm2 or p16INK4a loss. Genes Dev 2008; 22: 1337-1344.
8. Gaiddon C, Lokshin M, Ahn J, Zhang T, Prives C. A subset of tumor-derived mutant forms of p53 down-regulate p63 and p73 through a direct interaction with the p53 core domain. Mol Cell Biol 2001; 21: 1874-1887.
9. Flores ER, Sengupta S, Miller JB, Newman JJ, Bronson R, Crowley D et al. Tumor predisposition in mice mutant for p63 and p73: evidence for broader tumor suppressor functions for the p53 family. Cancer cell 2005; 7: 363-373.
10. Li Y, Prives C. Are interactions with p63 and p73 involved in mutant p53 gain of oncogenic function? Oncogene 2007; 26: 2220-2225.
11. Xu J, Reumers J, Couceiro JR, De Smet F, Gallardo R, Rudyak S et al. Gain of function of mutant p53 by coaggregation with multiple tumor suppressors. Nat Chem Biol 2011; 7: 285-295.
12. Walsh T, Casadei S, Lee MK, Pennil CC, Nord AS, Thornton AM et al. Mutations in genes for inherited ovarian, fallopian tube, and peritoneal carcinoma identified by massively parallel sequencing. Proc Natl Acad Sci USA 2011; 108: 18032-18037.
13. Barak Y, Juven T, Haffner R, Oren M. mdm2 expression is induced by wild type p53 activity. EMBO J 1993; 12: 461-468.
14. Meltzer PS. MDM2 and p53: a question of balance. J Natl Cancer Inst 1994; 86: 1265-1266.
15. Berghmans S, Murphey RD, Wienholds E, Neuberg D, Kutok JL, Fletcher CD et al. tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc Natl Acad Sci USA 2005; 102: 407-412.
16. Lee KC, Goh WL, Xu M, Kua N, Lunny D, Wong JS et al. Detection of the p53 response in zebrafish embryos using new monoclonal antibodies. Oncogene 2008; 27: 629-640.
17. Guo L, Chua J, Vijayakumar D, Lee KC, Lim K, Eng H et al. Detection of the 113p53 protein isoform: a p53-induced protein that feeds back on the p53 pathway to modulate the p53 response in zebrafish. Cell Cycle 2010; 9: 1998-2007.
18. Oliner JD, Pietenpol JA, Thiagalingam S, Gyuris J, Kinzler KW, Vogelstein B. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 1993; 362: 857-860.
19. Wang X. p53 regulation: teamwork between RING domains of Mdm2 and MdmX. Cell Cycle 2011; 10: 4225-4229.
20. Wang X, Wang J, Jiang X. MdmX protein is essential for Mdm2 protein-mediated p53 polyubiquitination. J Biol Chem 2011; 286: 23725-23734.
21. Fang S, Jensen JP, Ludwig RL, Vousden KH, Weissman AM. Mdm2 is a RING fingerdependent ubiquitin protein ligase for itself and p53. J Biol Chem 2000; 275: 8945-8951.
22. Plechanovova A, Jaffray EG, McMahon SA, Johnson KA, Navratilova I, Naismith JH et al. Mechanism of ubiquitylation by dimeric RING ligase RNF4. Nat Struct Mol Biol 2011; 18: 1052-1059.
23. Linke K, Mace PD, Smith CA, Vaux DL, Silke J, Day CL. Structure of the MDM2/MDMX RING domain heterodimer reveals dimerization is required for their ubiquitylation in trans. Cell Death Differ 2008; 15: 841-848.
24. Iyappan S, Wollscheid HP, Rojas-Fernandez A, Marquardt A, Tang HC, Singh RK et al. Turning the RING domain protein MdmX into an active ubiquitin-protein ligase. J Biol Chem 2010; 285: 33065-33072.
25. Robu ME, Larson JD, Nasevicius A, Beiraghi S, Brenner C, Farber SA et al. p53 activation by knockdown technologies. PloS Genet 2007; 3: e78.
26. Yang Y, Ludwig RL, Jensen JP, Pierre SA, Medaglia MV, Davydov IV et al. Small molecule inhibitors of HDM2 ubiquitin ligase activity stabilize and activate p53 in cells. Cancer cell 2005; 7: 547-559.
27. Ding K, Lu Y, Nikolovska-Coleska Z, Wang G, Qiu S, Shangary S et al. Structurebased design of spiro-oxindoles as potent, specific small-molecule inhibitors of the MDM2-p53 interaction. J Med Chem 2006; 49: 3432-3435.
28. Messner DJ, Romeo C, Boynton A, Rossie S. Inhibition of PP2A, but not PP5, mediates p53 activation by low levels of okadaic acid in rat liver epithelial cells. J Cell Biochem 2006; 99: 241-255.
29. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004; 303: 844-848.
30. van Leeuwen IM, Higgins M, Campbell J, Brown CJ, McCarthy AR, Pirrie L et al. Mechanism-specific signatures for small-molecule p53 activators. Cell Cycle 2011; 10: 1590-1598.
31. Suh YA, Post SM, Elizondo-Fraire AC, Maccio DR, Jackson JG, El-Naggar AK et al. multiple stress signals activate mutant p53 in vivo. Cancer Res 2011; 71: 7168-7175.
32. Zeng Z, Richardson J, Verduzco D, Mitchell DL, Patton EE. Zebrafish have a competent p53-dependent nucleotide excision repair pathway to resolve ultraviolet B-induced DNA damage in the skin. Zebrafish 2009; 6: 405-415.
33. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998; 273: 5858-5868.
34. Brooks CL, Gu W. p53 ubiquitination: Mdm2 and beyond. Mol Cell 2006; 21: 307-315.
35. Parant J, Chavez-Reyes A, Little NA, Yan W, Reinke V, Jochemsen AG et al. Rescue of embryonic lethality in Mdm4-null mice by loss of Trp53 suggests a nonoverlapping pathway with MDM2 to regulate p53. Nat Genet 2001; 29: 92-95.
36. Pant V, Xiong S, Iwakuma T, Quintas-Cardama A, Lozano G. Heterodimerization of Mdm2 and Mdm4 is critical for regulating p53 activity during embryogenesis but dispensable for p53 and Mdm2 stability. Proc Natl Acad Sci USA 2011; 108: 11995-12000.
37. Huang L, Yan Z, Liao X, Li Y, Yang J, Wang ZG et al. The p53 inhibitors MDM2/MDMX complex is required for control of p53 activity in vivo. Proc Natl Acad Sci USA 2011; 108: 12001-12006.
38. Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008; 319: 1352-1355.
39. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005; 434: 907-913.