Mdmx as an essential regulator of p53 activity

Biochemical and Biophysical Research Communications

Volumn 331, Issue 3, 2005, Pages 750-760

  Marine, Jean Christophe ^a   Jochemsen, Aart G ^b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Mdm2; Mdm4; Mdmx; p53; Tumorigenesis

Indexed keywords

AMINO ACID DERIVATIVE; DOXORUBICIN; PROTEIN HDMX S; PROTEIN INHIBITOR; PROTEIN MDM2; PROTEIN MDMX; PROTEIN P53; PROTEIN P53 INHIBITOR; REGULATOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; CANCER INHIBITION; CARCINOGENESIS; DNA DAMAGE; GENE AMPLIFICATION; GENE STRUCTURE; HUMAN; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; TRANSCRIPTION INITIATION;

MURINAE;

EID: 18144392733     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2005.03.151     Document Type: Review

References (76)

1. L. Cahilly-Snyder, T. Yang-Feng, U. Francke, and D.L. George Molecular analysis and chromosomal mapping of amplified genes isolated from a transformed mouse 3T3 cell line Somat. Cell Mol. Genet. 13 1987 235 244
2. J. Momand, G.P. Zambetti, D.C. Olson, D.L. George, and A.J. Levine The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation Cell 69 1992 1237 1245
3. J.D. Oliner, K.W. Kinzler, P.S. Meltzer, D.L. George, and B. Vogelstein Amplification of a gene encoding a p53-associated protein in human sarcomas Nature 358 1992 80 83
4. Y. Haupt, R. Maya, A. Kazaz, and M. Oren Mdm2 promotes the rapid degradation of p53 Nature 387 1997 296 299
5. M.H. Kubbutat, S.N. Jones, and K.H. Vousden Regulation of p53 stability by Mdm2 Nature 387 1997 299 303
6. R. Honda, H. Tanaka, and H. Yasuda Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53 FEBS Lett. 420 1997 25 27
7. R. Montes de Oca Luna, D.S. Wagner, and G. Lozano Rescue of early embryonic lethality in mdm2-deficient mice by absence of p53 Nature 378 1995 203 206
8. S.N. Jones, A.E. Roe, L.A. Donehower, and A. Bradley Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53 Nature 378 1995 206 208
9. U. Langheinrich, E. Hennen, G. Stott, and G. Vacun Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling Curr. Biol. 12 2002 2023 2028
10. S.M. Mendrysa, M.K. McElwee, J. Michalowski, K.A. O'Leary, K.M. Young, and M.E. Perry mdm2 is critical for inhibition of p53 during lymphopoiesis and the response to ionizing irradiation Mol. Cell. Biol. 23 2003 462 472
11. A. Shvarts, W.T. Steegenga, N. Riteco, T. van Laar, P. Dekker, M. Bazuine, R.C.A. van Ham, W. vander Houven van Oordt, G. Hateboer, A.J. van der Eb, and A.G. Jochemsen MDMX: a novel p53-binding protein with some functional properties of MDM2 EMBO J. 15 1996 5349 5357
12. A. Shvarts, M. Bazuine, P. Dekker, Y.F.M. Ramos, W.T. Steegenga, G. Merckx, R.C.A. van Ham, W. vander Houven van Oordt, A.J. van der Eb, and A.G. Jochemsen Isolation and identification of the human homolog of a new p53-binding protein, Mdmx Genomics 43 1997 34 42
13. D.A. Sharp, S.A. Kratowicz, M.J. Sank, and D.L. George Stabilization of the MDM2 oncoprotein by interaction with the structurally related MDMX protein J. Biol. Chem. 274 1999 38189 38196
14. S. Tanimura, S. Ohtsuka, K. Mitsui, K. Shirouzu, A. Yoshimura, and M. Ohtsubo MDM2 interacts with MDMX through their RING finger domains FEBS Lett. 447 1999 5 9
15. D.A. Freedman, C.B. Epstein, J.C. Roth, and A.J. Levine A genetic approach to mapping the p53 binding site in the MDM2 protein Mol. Med. 3 1997 248 259
16. M.W. Jackson, M.S. Lindstrom, and S.J. Berberich MdmX binding to ARF affects Mdm2 protein stability and p53 transactivation J. Biol. Chem. 276 2001 25336 25341
17. J.D. Weber, M.L. Kuo, B. Bothner, E.L. DiGiammarino, R.W. Kriwacki, M.F. Roussel, and C.J. Sherr Cooperative signals governing ARF-mdm2 interaction and nucleolar localization of the complex Mol. Cell. Biol. 20 2000 2517 2528
18. M.A. Lohrum, M. Ashcroft, M.H. Kubbutat, and K.H. Vousden Identification of a cryptic nucleolar-localization signal in MDM2 Nat. Cell Biol. 2 2000 179 181
19. X. Wang, J. Taplick, N. Geva, and M. Oren Inhibition of p53 degradation by Mdm2 acetylation FEBS Lett. 561 2004 195 201
20. S.N. Jones, M.A. Ansari-Lari, A.R. Hancock, W.J. Jones, R.A. Gibbs, L.A. Donehower, and A. Bradley Genomic organization of the mouse double minute 2 gene Gene 175 1996 209 213
21. R. Montes de Oca Luna, A.D. Tabor, H. Eberspaecher, D.L. Hulboy, L.L. Worth, M.S. Colman, C.A. Finlay, and G. Lozano The organization and expression of the mdm2 gene Genomics 33 1996 352 357
22. J.M. Parant, V. Reinke, B. Mims, and G. Lozano Organization, expression, and localization of the murine mdmx gene and pseudogene Gene 270 2001 277 283
23. X. Wu, J.H. Bayle, D. Olson, and A.J. Levine The p53-mdm-2 autoregulatory feedback loop Genes Dev. 7 1993 1126 1132
24. Y. Barak, T. Juven, R. Haffner, and M. Oren mdm2 expression is induced by wild type p53 activity EMBO J. 12 1993 461 468
25. T. Iwakuma, and G. Lozano MDM2, an introduction Mol. Cancer Res. 1 2003 993 1000
26. Y.F.M. Ramos, R. Stad, J. Attema, L.T.C. Peltenburg, A.J. van der Eb, and A.G. Jochemsen Aberrant expression of HDMX proteins in tumor cells correlates with wild-type p53 Cancer Res. 61 2001 1839 1842
27. R. Rallapalli, G. Strachan, B. Cho, W.E. Mercer, and D.J. Hall A novel MDMX transcript expressed in a variety of transformed cell lines encodes a truncated protein with potent p53 repressive activity J. Biol. Chem. 274 1999 8299 8308
28. J. Parant, A. Chavez-Reyes, N.A. Little, W. Yan, V. Reinke, A.G. Jochemsen, and G. Lozano Rescue of embryonic lethality in Mdm4-null mice by loss of Trp53 suggests a nonoverlapping pathway with MDM2 to regulate p53 Nat. Genet. 29 2001 92 95
29. D. Migliorini, E. Lazzerini-Denchi, D. Danovi, A.G. Jochemsen, M. Capillo, A. Gobbi, K. Helin, P.G. Pelicci, and J.C. Marine Mdm4 (Mdmx) regulates p53-induced growth arrest and neuronal cell death during early embryonic mouse development Mol. Cell. Biol. 22 2002 5527 5538
30. R.A. Finch, D.B. Donoviel, D. Potter, M. Shi, A. Fan, D.D. Freed, C.Y. Wang, B.P. Zambrowicz, R. Ramirez-Solis, A.T. Sands, and N. Zhang Mdmx is a negative regulator of p53 activity in vivo Cancer Res. 62 2002 3221 3225
31. J.C. Marine, and A.G. Jochemsen Mdmx and Mdm2: brothers in arms? Cell Cycle 3 2004 105 109
32. A. Martoriati, G. Doumont, M. Alcalay, E. Bellefroid, P.-G. Pelicci, and J.-C. Marine Dapk1, encoding an activator of a p19ARF-p53 mediated apoptotic checkpoint, is a transcription target of p53 Oncogene 24 2005 1461 1466
33. V. Bottger, A. Bottger, C. Garcia-Echeverria, Y.F.M. Ramos, A.J. van der Eb, A.G. Jochemsen, and D.P. Lane Comparative study of the p53-mdm2 and p53-DMX interfaces Oncogene 18 1999 189 199
34. P. Sabbatini, and F. McCormick MDMX inhibits the p300/CBP-mediated acetylation of p53 DNA Cell Biol. 21 2002 519 525
35. D. Danovi, E. Meulmeester, D. Pasini, D. Migliorini, M. Capra, S. Francoz, P. Gasparini, A. Gobbi, K. Helin, A. Jochemsen, P.G. Pelicci, and J.-C. Marine Amplification of Mdmx (or Mdm4) directly contributes to tumour formation by inhibiting p53-tumour suppressor activity Mol. Cell. Biol. 24 2004 5835 5843
36. C. Prives, and J.L. Manley Why is p53 acetylated? Cell 107 2001 815 818
37. M.W. Jackson, and S.J. Berberich MdmX protects p53 from Mdm2-mediated degradation Mol. Cell. Biol. 20 2000 1001 1007
38. R. Stad, Y.F.M. Ramos, N. Little, S. Grivell, J. Attema, A.J. van der Eb, and A.G. Jochemsen Hdmx stabilizes Mdm2 and p53 J. Biol. Chem. 275 2000 28039 28044
39. R. Stad, N.A. Little, D.P. Xirodimas, R. Frenk, A.J. van der Eb, D.P. Lane, M.K. Saville, and A.G. Jochemsen Mdmx stabilizes p53 and Mdm2 via two distinct mechanisms EMBO Rep. 2 2001 1029 1034
40. D. Migliorini, D. Danovi, E. Colombo, R. Carbone, P.G. Pelicci, and J.C. Marine Hdmx recruitment into the nucleus by Hdm2 is essential for its ability to regulate p53 stability and transactivation J. Biol. Chem. 277 2002 7318 7323
41. E. Meulmeester, R. Frenk, R. Stad, P. de Graaf, J.C. Marine, K.H. Vousden, and A.G. Jochemsen Critical role for a central part of Mdm2 in the ubiquitylation of p53 Mol. Cell. Biol. 23 2003 4929 4938
42. H. Kawai, D. Wiederschain, and Z.M. Yuan Critical contribution of the MDM2 acidic domain to p53 ubiquitination Mol. Cell. Biol. 23 2003 4939 4947
43. S.D. Boyd, K.Y. Tsai, and T. Jacks An intact HDM2 RING-finger domain is required for nuclear exclusion of p53 Nat. Cell Biol. 2 2000 563 568
44. R.K. Geyer, Z.K. Yu, and C.G. Maki The MDM2 RING-finger domain is required to promote p53 nuclear export Nat. Cell Biol. 2 2000 569 573
45. J. Gu, H. Kawai, L. Nie, H. Kitao, D. Wiederschain, A.G. Jochemsen, J. Parant, G. Lozano, and Z.M. Yuan Mutual dependence of MDM2 and MDMX in their functional inactivation of p53 J. Biol. Chem. 277 2002 19251 19254
46. L.K. Linares, A. Hengstermann, A. Ciechanover, S. Muller, and M. Scheffner HdmX stimulates Hdm2-mediated ubiquitination and degradation of p53 Proc. Natl. Acad. Sci. USA 100 2003 12009 12014
47. J. Roth, M. Dobbelstein, D.A. Freedman, T. Shenk, and A.J. Levine Nucleo-cytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of the p53 protein via a pathway used by the human immunodeficiency virus rev protein EMBO J. 17 1998 554 564
48. C. Li, L. Chen, and J. Chen DNA damage induces MDMX nuclear translocation by p53-dependent and -independent mechanisms Mol. Cell. Biol. 22 2002 7562 7571
49. P. de Graaf, N.A. Little, Y.F.M. Ramos, E. Meulmeester, S.J. Letteboer, and A.G. Jochemsen Hdmx protein stability is regulated by the ubiquitin ligase activity of Mdm2 J. Biol. Chem. 278 2003 38315 38324
50. Y. Pan, and J. Chen MDM2 promotes ubiquitination and degradation of MDMX Mol. Cell. Biol. 23 2003 5113 5121
51. H. Kawai, D. Wiederschain, H. Kitao, J. Stuart, K.K. Tsai, and Z.M. Yuan DNA damage-induced MDMX degradation is mediated by MDM2 J. Biol. Chem. 278 2003 45946 45953
52. Y. Pereg, D. Shkedy, P. de Graaf, E. Meulmeester, M. Edelson-Averbukh, M. Salek, S. Biton, A.F. Teunisse, W.D. Lehmann, A.G. Jochemsen, and Y. Shiloh Phosphorylation of Hdmx mediates its Hdm2- and ATM-dependent degradation in response to DNA damage Proc. Natl. Acad. Sci. USA 2005
53. L.J. Saucedo, C.D. Myers, and M.E. Perry Multiple murine double minute gene 2 (MDM2) proteins are induced by ultraviolet light J. Biol. Chem. 274 1999 8161 8168
54. M.E. Perry, S.M. Mendrysa, L.J. Saucedo, P. Tannous, and M. Holubar p76(MDM2) inhibits the ability of p90(MDM2) to destabilize p53 J. Biol. Chem. 275 2000 5733 5738
55. F. Gentiletti, F. Mancini F, M. D'Angelo, A. Sacchi, A. Pontecorvi, A.G. Jochemsen, and F. Moretti MDMX stability is regulated by p53-induced caspase cleavage in NIH3T3 mouse fibroblasts Oncogene 21 2002 867 877
56. F. Mancini, F. Gentiletti, M. D'Angelo, S. Giglio, S. Nanni, C. D'Angelo, A. Farsetti, G. Citro, A. Sacchi, A. Pontecorvi, and F. Moretti MDM4 (MDMX) overexpression enhances stabilization of stress-induced p53 and promotes apoptosis J. Biol. Chem. 279 2004 8169 8180
57. M.J. Riemenschneider, R. Buschges, M. Wolter, J. Reifenberger, J. Bostrom, J.A. Kraus, U. Schlegel, and G. Reifenberger Amplification and overexpression of the MDM4 (MDMX) gene from 1q32 in a subset of malignant gliomas without TP53 mutation or MDM2 amplification Cancer Res. 59 1999 6091 6096
58. M.J. Riemenschneider, C.B. Knobbe, and G. Reifenberger Refined mapping of 1q32 amplicons in malignant gliomas confirms MDM4 as the main amplification target Int. J. Cancer 104 2003 752 757
59. L.T. Vassilev, B.T. Vu, B. Graves, D. Carvajal, F. Podlaski, Z. Filipovic, N. Kong, U. Kammlott, C. Lukacs, C. Klein, N. Fotouhi, and E.A. Liu In vivo activation of the p53 pathway by small-molecule antagonists of MDM2 Science 303 2004 844 848
60. F. Bartel, L.C. Harris, P. Wurl, and H. Taubert MDM2 and its splice variant messenger RNAs: expression in tumors and down-regulation using antisense oligonucleotides Mol. Cancer Res. 2 2004 29 35
61. R. Rallapalli, G. Strachan, R.S. Tuan, and D.J. Hall Identification of a domain within MDMX-S that is responsible for its high affinity interaction with p53 and high-level expression in mammalian cells J. Cell. Biochem. 89 2003 563 575
62. M. Li, D. Chen, A. Shiloh, J. Luo, A.Y. Nikolaev, J. Qin, and W. Gu Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization Nature 416 2002 648 653
63. M. Li, C.L. Brooks, N. Kon, and W. Gu A dynamic role of HAUSP in the p53-Mdm2 pathway Mol. Cell 13 2004 879 886
64. J.M. Cummins, C. Rago, M. Kohli, K.W. Kinzler, C. Lengauer, and B. Vogelstein Tumour suppression: disruption of HAUSP gene stabilizes p53 Nature 428 2004 1 p following 486
65. G. Ganguli, and B. Wasylyk p53-independent functions of MDM2 Mol. Cancer Res. 1 2003 1027 1035
66. W.M. Ongkeko, X.Q. Wang, W.Y. Siu, A.W. Lau, K. Yamashita, A.L. Harris, L.S. Cox, and R.Y. Poon MDM2 and MDMX bind and stabilize the p53-related protein p73 Curr. Biol. 9 1999 829 832
67. X. Wang, T. Arooz, W.Y. Siu, C.H. Chiu, A. Lau, K. Yamashita, and R.Y. Poon MDM2 and MDMX can interact differently with ARF and members of the p53 family FEBS Lett. 490 2001 202 208
68. E.R. Flores, K.Y. Tsai, D. Crowley, S. Sengupta, A. Yang, F. McKeon, and T. Jacks p63 and p73 are required for p53-dependent apoptosis in response to DNA damage Nature 416 2002 560 564
69. M. Senoo, J.P. Manis, F.W. Alt, and F. McKeon p63 and p73 are not required for the development and p53-dependent apoptosis of T cells Cancer Cell 6 2004 85 89
70. N.A. Little, and A.G. Jochemsen Hdmx and Mdm2 can repress transcription activation by p53 but not by p63 Oncogene 20 2001 4576 4580
71. M. Kadakia, C. Slader, and S.J. Berberich Regulation of p63 function by Mdm2 and MdmX DNA Cell Biol. 20 2001 321 330
72. M.W. Jackson, M.S. Lindstrom, and S.J. Berberich MdmX binding to ARF affects Mdm2 protein stability and p53 transactivation J. Biol. Chem. 276 2001 25336 25341
73. K. Lundgren, R. Montes de Oca Luna, Y.B. McNeill, E.P. Emerick, B. Spencer, C.R. Barfield, G. Lozano, M.P. Rosenberg, and C.A. Finlay Targeted expression of MDM2 uncouples S phase from mitosis and inhibits mammary gland development independent of p53 Genes Dev. 11 1997 714 725
74. M. Alkhalaf, G. Ganguli, N. Messaddeq, M. Le Meur, and B. Wasylyk MDM2 overexpression generates a skin phenotype in both wild type and p53 null mice Oncogene 18 1999 1419 1434
75. R.L. Phillips, R.E. Ernst, B. Brunk, N. Ivanova, M.A. Mahan, J.K. Deanehan, K.A. Moore, G.C. Overton, and I.R. Lemischka The genetic program of hematopoietic stem cells Science 288 2000 1635 1640
76. S.N. Jones, A.R. Hancock, H. Vogel, L.A. Donehower, and A. Bradley Overexpression of Mdm2 in mice reveals a p53-independent role for Mdm2 in tumorigenesis Proc. Natl. Acad. Sci. USA 95 1998 15608 15612