Tumor suppressor protein Pdcd4 interacts with Daxx and modulates the stability of Daxx and the Hipk2-dependent phosphorylation of p53 at serine 46

Oncogenesis

Volumn 2, Issue , 2013, Pages

  Kumar, N ^a   Wethkamp, N ^a   Waters, L C ^b   Carr, M D ^b   Klempnauer, K H ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Daxx; p53; Pdcd4; protein protein interaction

Indexed keywords

DAXX PROTEIN; HOMEODOMAIN INTERACTING PROTEIN KINASE 2; PROGRAMMED CELL DEATH 4 PROTEIN; PROTEIN P53; SERINE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; GENOTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; ULTRAVIOLET IRRADIATION;

EID: 84880534053     PISSN: None     EISSN: 21579024     Source Type: Journal    
DOI: 10.1038/oncsis.2012.37     Document Type: Article

References (73)

1. Shibahara K, Asano M, Ishida Y, Aoki T, Koike T, Honjo T. Isolation of a novel mouse gene MA-3 that is induced upon programmed cell death. Gene 1995; 166: 297-301. (Pubitemid 26007637)
2. Cmarik JL, Min H, Hegamyer G, Zhan S, Kulesz-Martin M, Yoshinaga H et al. Differentially expressed protein Pdcd4 inhibits tumor promoter-induced neoplastic transformation. Proc Natl Acad Sci USA 1999; 96: 14037-14042.
3. Jansen AP, Camalier CE, Colburn NH. Epidermal expression of the translation inhibitor programmed cell death 4 suppresses tumorigenesis. Cancer Res 2005; 65: 6034-6041. (Pubitemid 40994387)
4. Chen Y, Knosel T, Kristiansen G, Pietas A, Garber ME, Matsuhashi S et al. Loss of PDCD4 expression in human lung cancer correlates with tumour progression and prognosis. J Pathol 2003; 200: 640-646. (Pubitemid 36987314)
5. Afonja O, Juste D, Das S, Matsuhashi S, Samuels HH. Induction of PDCD4 tumor suppressor gene expression by RAR agonists, antiestrogen and HER-2/neu antagonist in breast cancer cells. Evidence for a role in apoptosis. Oncogene 2004; 23: 8135-8145. (Pubitemid 39531854)
6. Zhang H, Ozaki I, Mizuta T, Hamajima H, Yasutake T, Eguchi Y et al. Involvement of programmed cell death 4 in transforming growth factor-beta1-induced apoptosis in human hepatocellular carcinoma. Oncogene 2006; 25: 6101-6112. (Pubitemid 44562408)
7. Mudduluru G, Medved F, Grobholz R, Jost C, Gruber A, Leupold JH et al. Loss of programmed cell death 4 expression marks adenoma-carcinoma transition, correlates inversely with phosphorylated protein kinase B, and is an independent prognostic factor in resected colorectal cancer. Cancer 2007; 110: 1697-1707. (Pubitemid 47558956)
8. Wang Q, Sun Z, Yang H-S. Downregulation of tumour suppressor Pdcd4 promotes invasion and activates both b-catenin/TCF and AP-1-dependent transcription in colon carcinoma cells. Oncogene 2008; 27: 1527-1535. (Pubitemid 351347877)
9. Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, Lund AH. Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem 2008; 283: 1026-1033.
10. Lu Z, Liu M, Stribinskis V, Klinge CM, Ramos KS, Colburn NH. MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene 2008; 27: 4373-4379. (Pubitemid 352010003)
11. Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, Post S et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 2008; 27: 2128-2136. (Pubitemid 351485639)
12. Dorello NV, Peschiaroli A, Guardavaccaro D, Colburn NH, Sherman NE, Pagano M. S6K1-and betaTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth. Science 2006; 314: 467-471. (Pubitemid 44628968)
13. Schmid T, Jansen AP, Baker AR, Hegamyer G, Hagan JP, Colburn NH. Translation inhibitor Pdcd4 is targeted for degradation during tumor promotion. Cancer Res 2008; 68: 1254-1260. (Pubitemid 351346830)
14. Yang HS, Matthews CP, Clair T, Wang Q, Baker AR, Li CC et al. Tumorigenesis suppressor Pdcd4 down-regulates mitogen-activated protein kinase kinase kinase kinase 1 expression to suppress colon carcinoma cell invasion. Mol Cell Biol 2006; 26: 1297-1306. (Pubitemid 43202557)
15. Leupold JH, Yang HS, Colburn NH, Asangani I, Post S, Allgayer H. Tumor suppressor Pdcd4 inhibits invasion/intravasation and regulates urokinase receptor (u-PAR) gene expression via Sp-transcription factors. Oncogene 2007; 26: 4550-4562. (Pubitemid 47039134)
16. Bitomsky N, Wethkamp N, Marikkannu R, Klempnauer K-H. siRNA-mediated knock-down of Pdcd4 expression causes up-regulation of p21(Waf1/Cip1) expression. Oncogene 2008; 27: 4820-4829.
17. Singh P, Marikkannu R, Bitomsky N, Klempnauer K-H. Disruption of the Pdcd4 tumor suppressor gene in chicken DT40 cells reveals its role in the DNA-damage response. Oncogene 2009; 28: 3758-3764.
18. Böhm M, Sawicka K, Siebrasse JP, Brehmer-Fastnacht A, Peters R, Klempnauer K-H. The transformation suppressor protein Pdcd4 shuttles between nucleus and cytoplasm and binds RNA. Oncogene 2003; 22: 4905-4910. (Pubitemid 36981280)
19. Wedeken L, Ohnheiser J, Hirschi B, Wethkamp N, Klempnauer K-H. Association of tumor suppressor protein Pdcd4 with ribosomes is mediated by protein-protein and protein-RNA interactions. Genes Cancer 2010; 1: 293-301.
20. Palamarchuk A, Efanov A, Maximov V, Aqeilan RI, Croce CM, Pekarsky Y. Akt phosphorylates and regulates Pdcd4 tumor suppressor protein. Cancer Res 2005; 65: 11282-11286. (Pubitemid 41821683)
21. Yang HS, Knies JL, Stark C, Colburn NH. Pdcd4 suppresses tumor phenotype in JB6 cells by inhibiting AP-1 transactivation. Oncogene 2003; 22: 3712-3720. (Pubitemid 36760733)
22. Bitomsky N, Böhm M, Klempnauer K-H. Transformation suppressor protein Pdcd4 interferes with JNK-mediated phosphorylation of c-Jun and recruitment of the coactivator p300 by c-Jun. Oncogene 2004; 23: 7484-7493. (Pubitemid 39389690)
23. Yang HS, Jansen AP, Komar AA, Zheng X, Merrick WC, Costes S et al. The transformation suppressor Pdcd4 is a novel eukaryotic translation initiation factor 4A binding protein that inhibits translation. Mol Cell Biol 2003; 23: 26-37. (Pubitemid 36008498)
24. Yang HS, Cho MH, Zacowicz H, Hegamyer G, Sonenberg N, Colburn N. A novel function of the MA-3 domains in transformation and translation suppressor Pdcd4 is essential for its binding to eukaryotic translation initiation factor 4A. Mol Cell Biol 2004; 24: 3894-3906. (Pubitemid 38496167)
25. LaRonde-LeBlanc N, Santhanam AN, Baker AR, Wlodawer A, Colburn NH. Structural basis for inhibition of translation by the tumor suppressor Pdcd4. Mol Cell Biol 2007; 27: 147-156. (Pubitemid 46013240)
26. Waters LC, Veverka V, Böhm M, Schmedt T, Choong PT, Muskett FW et al. Structure of the C-terminal MA-3 domain of the tumour suppressor protein Pdcd4 and characterization of its interaction with eIF4A. Oncogene 2007; 26: 4941-4950. (Pubitemid 47172651)
27. Suzuki C, Garces RG, Edmonds KA, Hiller S, Hyberts SG, Marintchev A et al. PDCD4 inhibits translation initiation by binding to eIF4A using both its MA3 domains. Proc Natl Acad Sci USA 2008; 105: 3274-3279. (Pubitemid 351723543)
28. Chang JH, Cho YH, Sohn SY, Choi JM, Kim A, Kim YC et al. Cyrstal structure of the eIF4A-PDCD4 complex. Proc Natl Acad Sci USA 2009; 106: 3148-3153.
29. Loh PG, Yang HS, Walsh MA, Wang Q, Wang X, Cheng Z et al. Structural basis for translational inhibition by the tumour suppressor Pdcd4. EMBO J 2009; 28: 274-285.
30. Waters LC, Strong SL, Ferlemann E, Oka O, Muskett FW, Veverka V et al. Structure of the tandem MA-3 region of Pdcd4 protein and characterization of its interactions with eIF4A and eIF4G: molecular mechanisms of a tumor suppressor. J Biol Chem 2011; 286: 17270-17280.
31. Singh P, Wedeken L, Waters LC, Carr MD, Klempnauer K-H. Pdcd4 directly binds the coding region of c-myb mRNA and suppresses its translation. Oncogene 2011; 30: 4864-4873.
32. Wedeken L, Singh P, Klempnauer K-H. Tumor suppressor protein Pdcd4 inhibits translation of p53 mRNA. J Biol Chem 2011; 286: 42855-42862.
33. Eto K, Goto S, Nakashima W, Ura Y, Abe SI. Loss of programmed cell death 4 induces apoptosis by promoting the translation of procaspase-3 mRNA. Cell Death Differ 2012; 19: 573-581.
34. Yang X, Khosravi-Far R, Chang HY, Baltimore D. Daxx a novel Fas-binding protein that activates JNK and apoptosis. Cell 1997; 89: 1067-1076. (Pubitemid 127678740)
35. Perlman R, Schiemann WP, Brooks MW, Lodish HF, Weinberg RA. TGF-betainduced apoptosis is mediated by the adapter protein Daxx that facilitates JNK activation. Nat Cell Biol 2001; 3: 708-714. (Pubitemid 32734248)
36. Chen LY, Chen JD. Daxx silencing sensitizes cells to multiple apoptotic pathways. Mol Cell Biol 2003; 23: 7108-7121. (Pubitemid 37210994)
37. Michaelson JS, Bader D, Kuo F, Kozak C, Lder P. Loss of Daxx, a promiscuously interacting protein, results in extensive apoptosis in early mouse development. Genes Dev 1999; 13: 1918-1923. (Pubitemid 29407359)
38. Ishov AM, Sotnikov AG, Negorev D, Vladimirova OV, Neff N, Kamitani T et al. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J Cell Biol 1999; 147: 221-234.
39. Lin DY, Huang YS, Jeng JC, Kuo HY, Chang CC, Chao TT et al. Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol Cell 2006; 24: 341-354.
40. Wethkamp N, Hanenberg H, Funke S, Suschek CV, Wetzel W, Heikaus S et al. Daxx-beta and Daxx-gamma, two novel splice variants of the transcriptional co-repressor Daxx. J Biol Chem 2011; 286: 19576-19588.
41. Puto LA, Reed JC. Daxx represses RelB target promoters via DNA methyltransferase recruitment and DNA hypermethylation. Genes Dev 2008; 22: 998-1010. (Pubitemid 351544239)
42. Li R, Pei H, Watson DK, Papas TS. EAP1/Daxx interacts with ETS1 and represses transcriptional activation of ETS1 target genes. Oncogene 2000; 19: 745-753. (Pubitemid 30107705)
43. Lehembre F, Muller S, Pandolfi PP, Dejean A. Regulation of Pax3 transcriptional activity by SUMO-1-modified PML. Oncogene 2001; 20: 1-9. (Pubitemid 32142332)
44. Lin DY, Fang HI, Ma AH, Huang YS, Pu YS, Jenster G et al. Negative modulation of androgen receptor transcriptional activity by Daxx. Mol Cell Biol 2004; 24: 10529-10541. (Pubitemid 39603115)
45. Chang CC, Lin DY, Fang HI, Chen RH, Shih HM. Daxx mediates the small ubiquitinlike modifier-dependent transcriptional repression of Smad4. J Biol Chem 2005; 280: 10164-10173.
46. Kuo HY, Chang CC, Jeng JC, Hu HM, Lin DY, Maul GG et al. SUMO modification negatively modulates the transcriptional activity of CREB-binding protein via the recruitment of Daxx. Proc Natl Acad Sci USA 2005; 102: 16973-16978. (Pubitemid 41692668)
47. Wethkamp N, Klempnauer K-H. Daxx is a transcriptional repressor of CCAAT/enhancer-binding protein beta. J Biol Chem 2009; 284: 28783-28794.
48. Shih HM, Chang CC, Kuo HY, Lin DY. Daxx mediates SUMO-dependent transcriptional control and subnuclear compartmentalization. Biochem Soc Trans 2007; 35: 1397-1400.
49. Li Q, Wang X, Wu X, Rui Y, Liu W, Wang J et al. Daxx cooperates with the Axin/Hipk2/p53 complex to induce cell death. Cancer Res 2007; 67: 66-74. (Pubitemid 46142760)
50. Tang J, Qu LK, Zhang J, Wang W, Michaelson JS, Degenhardt YY et al. Critical role for Daxx in regulating Mdm2. Nat Cell Biol 2006; 8: 855-862. (Pubitemid 44151589)
51. Song MS, Song SJ, Kim SY, Oh HJ, Lim DS. The tumour suppressor RASSF1A promotes MDM2 self-ubiquitination by disrupting the MDM2-DAXX-HAUSP complex. EMBO J 2008; 27: 1863-1874.
52. Tang J, Qu L, Pang M, Yang X. Daxx is reciprocally regulated by Mdm2 and Hausp. Biochem Biophys Res Commun 2010; 393: 542-545.
53. Song MS, Salmena L, Carracedo A, Egia A, Lo-Coco F, Teruya-Feldstein J et al. The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network. Nature 2008; 455: 813-817.
54. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 2010; 140: 678-691.
55. Drané P, Ouararhni K, Depaux A, Shuaib M, Hamiche A. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 2010; 24: 1253-1265.
56. Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication- independent chromatin assembly at telomeres. Proc Natl Acad Sci USA 2010; 107: 14075-14080.
57. Weidtkamp-Peters S, Lenser T, Negorev D, Gerstner N, Hofmann TG, Schwanitz G et al. Dynamics of component exchange at PML nuclear bodies. J Cell Sci 2008; 121: 2731-2743.
58. D'Orazi G, Cecchinelli B, Bruno T, Manni I, Higashimoto Y, Saito S et al. Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat Cell Biol 2002; 4: 11-19.
59. Winter M, Sombroek D, Dauth I, Moehlenbrink J, Scheuermann K, Crone J et al. Control of HIPK2 stability by ubiquitin ligase Siah-1 and checkpoint kinases ATM and ATR. Nat Cell Biol 2008; 10: 812-824. (Pubitemid 351927710)
60. Dyson HJ, Wright PE. Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 2005; 6: 197-208. (Pubitemid 40314921)
61. Wright PE, Dyson HJ. Linking folding and binding. Curr Opin Struct Biol 2009; 19: 31-38.
62. Zhu J, Zhou J, Peres L, Riaucoux F, Honoré N, Kogan S et al. A sumoylation site in PML/RARA is essential for leukemic transformation. Cancer Cell 2005; 7: 143-153. (Pubitemid 40248340)
63. Calzado MA, Renner F, Roscic A, Schmitz ML. HIPK2: a versatile switchboard regulating the transcription machinery and cell death. Cell Cycle 2007; 6: 139-143. (Pubitemid 46232491)
64. Rinaldo C, Prodosmo A, Siepi F, Soddu S. HIPK2: a multitalented partner for transcription factors in DNA damage response and development. Biochem Cell Biol 2007; 85: 411-418. (Pubitemid 47518036)
65. Bensaad K, Vousden KH. P53: new roles in metabolism. Trends Cell Biol 2007; 17: 286-291. (Pubitemid 46829848)
66. Vousden KH, Lane DP. p53 in health and disease. Nat Rev Cancer 2007; 8: 275-283. (Pubitemid 46474662)
67. Mathew R, Karandza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer 2007; 7: 961-967. (Pubitemid 350165856)
68. Green DR, Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 2009; 458: 1127-1130.
69. Vousden KH, Ryan KM. p53 and metabolism. Nat Rev Cancer 2009; 9: 691-700.
70. Meulmeester E, Maurice MM, Boutell C, Teunisse AF, Ovaa H, Abraham TE et al. Loss of HAUSP-mediated deubiquitination contributes to DNA damage-induced destabilization of Hdmx and Hdm2. Mol Cell 2005; 18: 565-576. (Pubitemid 40726233)
71. Muromoto R, Sugiyama K, Yamamoto T, Oritani K, Shimoda K, Matsuda T. Physical and functional interactions between Daxx and TSG101. Biochem Biophys Res Commun 2004; 316: 827-833. (Pubitemid 38368027)
72. Hofmann TG, Mö ller A, Sirma H, Zentgraf H, Taya Y, Dröge W et al. Regulation of p53 activity by its interaction with homeodomain-interacting protein kinase-2. Nat Cell Biol 2002; 4: 1-10. (Pubitemid 34071974)
73. Mink S, Haenig B, Klempnauer K-H. Interaction and functional collaboration of p300 and C/EBPbeta. Mol Cell Biol 1997; 17: 6609-6617. (Pubitemid 27451207)