Tetramerization-defects of p53 result in aberrant ubiquitylation and transcriptional activity

Molecular Oncology

Volumn 8, Issue 5, 2014, Pages 1026-1042

  Lang, Valérie ^a   Pallara, Chiara ^b   Zabala, Amaia ^c   Lobato Gil, Sofia ^a   Lopitz Otsoa, Fernando ^c   Farrás, Rosa ^d   Hjerpe, Roland ^c,f   Torres Ramos, Monica ^c,i   Zabaleta, Lorea ^a   Blattner, Christine ^e   Hay, Ronald T ^f   Barrio, Rosa ^c   Carracedo, Arkaitz ^c,g,h   Fernandez Recio, Juan ^b   Rodríguez, Manuel S ^a   Aillet, Fabienne ^a  

^a San Sebastian Donostia   (Spain)

^b BARCELONA SUPERCOMPUTING CENTER   (Spain)

^c CIC BIOGUNE   (Spain)

^d CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^e KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^f UNIVERSITY OF DUNDEE   (United Kingdom)

^g BASQUE FOUNDATION FOR SCIENCE   (Spain)

^h UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

ⁱ NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

Author keywords

Oligomerization; P53; Proteasome; Transcription; Ubiquitylation

Indexed keywords

ARGININE; DOXORUBICIN; LEUCINE; PROTEASOME; PROTEIN BAX; PROTEIN MDM2; PROTEIN P53; PUMA PROTEIN; TETRAMER; MDM2 PROTEIN, HUMAN;

AMINO ACID SUBSTITUTION; ARTICLE; CANCER CHEMOTHERAPY; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; LUNG CANCER CELL LINE; MCF 7 CELL LINE; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR MODEL; MUTANT; OLIGOMERIZATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; TRANSCRIPTION INITIATION; UBIQUITINATION; WILD TYPE; CHEMISTRY; GENETICS; METABOLISM; PROTEIN MULTIMERIZATION; SITE DIRECTED MUTAGENESIS; TUMOR CELL LINE; APOPTOSIS; HYDROPHOBICITY; MOLECULAR PATHOLOGY; PROTEIN MODIFICATION; PROTEIN STRUCTURE; TETRAMERIZATION; TRANSCRIPTION REGULATION;

CELL LINE, TUMOR; HUMANS; MOLECULAR DOCKING SIMULATION; MUTAGENESIS, SITE-DIRECTED; POINT MUTATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN MULTIMERIZATION; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-MDM2; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITINATION;

EID: 84903537605     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.04.002     Document Type: Article

References (54)

1. Aillet F., Lopitz-Otsoa F., Hjerpe R., Torres-Ramos M., Lang V., Rodriguez M.S. Isolation of ubiquitylated proteins using tandem ubiquitin-binding entities. Methods Mol Biol 2012, 832:173-183.
2. Alarcon-Vargas D., Ronai Z. SUMO in cancer-wrestlers wanted. Cancer Biol. Ther. 2002, 1:237-242.
3. Asher G., Reuven N., Shaul Y. 20S proteasomes and protein degradation "by default". BioEssays: News Rev. Mol. Cell. Dev. Biol. 2006, 28:844-849.
4. Blattner C., Knebel A., Radler-Pohl A., Sachsenmaier C., Herrlich P., Rahmsdorf H.J. DNA damaging agents and growth factors induce changes in the program of expressed gene products through common routes. Environ. Mol. Mutagen. 1994, 24:3-10.
5. Canutescu A.A., Shelenkov A.A., Dunbrack R.L. A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci.: Publ. Protein Soc. 2003, 12:2001-2014.
6. Case D.A., Cheatham T.E., Darden T., Gohlke H., Luo R., Merz K.M., Onufriev A., Simmerling C., Wang B., Woods R.J. The Amber biomolecular simulation programs. J. Comput. Chem. 2005, 26:1668-1688.
7. Catic A., Suh C.Y., Hill C.T., Daheron L., Henkel T., Orford K.W., Dombkowski D.M., Liu T., Liu X.S., Scadden D.T. Genome-wide map of nuclear protein degradation shows NCoR1 turnover as a key to mitochondrial gene regulation. Cell 2013, 155:1380-1395.
8. Chene P. Semiquantitative comparison of the DNA-binding activity of in vitro-synthesized proteins. BioTechniques 1997, 23:792-794.
9. Chene P., Bechter E. Cellular characterisation of p53 mutants with a single missense mutation in the beta-strand 326-333 and correlation of their cellular activities with in vitro properties. J. Mol. Biol. 1999, 288:891-897.
10. Chene P., Mittl P., Grutter M. In vitro structure-function analysis of the beta-strand 326-333 of human p53. J. Mol. Biol. 1997, 273:873-881.
11. Cheng T.M., Blundell T.L., Fernandez-Recio J. pyDock: electrostatics and desolvation for effective scoring of rigid-body protein-protein docking. Proteins 2007, 68:503-515.
12. Chowdary D.R., Dermody J.J., Jha K.K., Ozer H.L. Accumulation of p53 in a mutant cell line defective in the ubiquitin pathway. Mol. Cell. Biol. 1994, 14:1997-2003.
13. Chuikov S., Kurash J.K., Wilson J.R., Xiao B., Justin N., Ivanov G.S., McKinney K., Tempst P., Prives C., Gamblin S.J., Barlev N.A., Reinberg D. Regulation of p53 activity through lysine methylation. Nature 2004, 432:353-360.
14. Clore G.M., Ernst J., Clubb R., Omichinski J.G., Kennedy W.M., Sakaguchi K., Appella E., Gronenborn A.M. Refined solution structure of the oligomerization domain of the tumour suppressor p53. Nat. Struct. Biol. 1995, 2:321-333.
15. Duddy P.M., Hanby A.M., Barnes D.M., Camplejohn R.S. Improving the detection of p53 mutations in breast cancer by use of the FASAY, a functional assay. J. Mol. Diagn.: JMD 2000, 2:139-144.
16. Fang S., Jensen J.P., Ludwig R.L., Vousden K.H., Weissman A.M. Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J. Biol. Chem. 2000, 275:8945-8951.
17. Feng L., Lin T., Uranishi H., Gu W., Xu Y. Functional analysis of the roles of posttranslational modifications at the p53 C terminus in regulating p53 stability and activity. Mol. Cell. Biol. 2005, 25:5389-5395.
18. Friedman P.N., Chen X., Bargonetti J., Prives C. The p53 protein is an unusually shaped tetramer that binds directly to DNA. Proc. Natl. Acad. Sci. U S A 1993, 90:3319-3323.
19. Funk W.D., Pak D.T., Karas R.H., Wright W.E., Shay J.W. A transcriptionally active DNA-binding site for human p53 protein complexes. Mol. Cell. Biol. 1992, 12:2866-2871.
20. Gabb H.A., Jackson R.M., Sternberg M.J. Modelling protein docking using shape complementarity, electrostatics and biochemical information. J. Mol. Biol. 1997, 272:106-120.
21. Hjerpe R., Aillet F., Lopitz-Otsoa F., Lang V., England P., Rodriguez M.S. Efficient protection and isolation of ubiquitylated proteins using tandem ubiquitin-binding entities. EMBO Rep. 2009, 10:1250-1258.
22. Hjerpe R., Aillet F., Lopitz-Otsoa F., Lang V., Torres-Ramos M., Farras R., Hay R.T., Rodriguez M.S. Oligomerization conditions Mdm2-mediated efficient p53 polyubiquitylation but not its proteasomal degradation. Int. J. Biochem. Cell Biol. 2010, 42:725-735.
23. Hollstein M., Sidransky D., Vogelstein B., Harris C.C. p53 mutations in human cancers. Science 1991, 253:49-53.
24. Jeffrey P.D., Gorina S., Pavletich N.P. Crystal structure of the tetramerization domain of the p53 tumor suppressor at 1.7 angstroms. Science 1995, 267:1498-1502.
25. Kato S., Han S.Y., Liu W., Otsuka K., Shibata H., Kanamaru R., Ishioka C. Understanding the function-structure and function-mutation relationships of p53 tumor suppressor protein by high-resolution missense mutation analysis. Proc. Natl. Acad. Sci. U S A 2003, 100:8424-8429.
26. Kawaguchi T., Kato S., Otsuka K., Watanabe G., Kumabe T., Tominaga T., Yoshimoto T., Ishioka C. The relationship among p53 oligomer formation, structure and transcriptional activity using a comprehensive missense mutation library. Oncogene 2005, 24:6976-6981.
27. Kopp F., Oak P.S., Wagner E., Roidl A. miR-200c sensitizes breast cancer cells to doxorubicin treatment by decreasing TrkB and Bmi1 expression. PloS One 2012, 7:e50469.
28. Krummel K.A., Lee C.J., Toledo F., Wahl G.M. The C-terminal lysines fine-tune P53 stress responses in a mouse model but are not required for stability control or transactivation. Proc. Natl. Acad. Sci. U S A 2005, 102:10188-10193.
29. Le Cam L., Linares L.K., Paul C., Julien E., Lacroix M., Hatchi E., Triboulet R., Bossis G., Shmueli A., Rodriguez M.S., Coux O., Sardet C. E4F1 is an atypical ubiquitin ligase that modulates p53 effector functions independently of degradation. Cell 2006, 127:775-788.
30. Lee W., Harvey T.S., Yin Y., Yau P., Litchfield D., Arrowsmith C.H. Solution structure of the tetrameric minimum transforming domain of p53. Nat. Struct. Biol. 1994, 1:877-890.
31. Levine A.J. p53, the cellular gatekeeper for growth and division. Cell 1997, 88:323-331.
32. Maki C.G. Oligomerization is required for p53 to be efficiently ubiquitinated by MDM2. J. Biol. Chem. 1999, 274:16531-16535.
33. Maki C.G., Howley P.M. Ubiquitination of p53 and p21 is differentially affected by ionizing and UV radiation. Mol. Cell. Biol. 1997, 17:355-363.
34. Maki C.G., Huibregtse J.M., Howley P.M. In vivo ubiquitination and proteasome-mediated degradation of p53(1). Cancer Res. 1996, 56:2649-2654.
35. Maltzman W., Czyzyk L. UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol. Cell. Biol. 1984, 4:1689-1694.
36. Mateu M.G., Fersht A.R. Nine hydrophobic side chains are key determinants of the thermodynamic stability and oligomerization status of tumour suppressor p53 tetramerization domain. EMBO J. 1998, 17:2748-2758.
37. McShane E., Selbach M. Gene expression: degrade to derepress. EMBO J. 2014, 33:407-408.
38. Mehrpour M., Esclatine A., Beau I., Codogno P. Overview of macroautophagy regulation in mammalian cells. Cell Res. 2010, 20:748-762.
39. Meyer T., D'Abramo M., Hospital A., Rueda M., Ferrer-Costa C., Perez A., Carrillo O., Camps J., Fenollosa C., Repchevsky D., Gelpi J.L., Orozco M. MoDEL (Molecular Dynamics Extended Library): a database of atomistic molecular dynamics trajectories. Structure 2010, 18:1399-1409.
40. Miller M., Lubkowski J., Rao J.K., Danishefsky A.T., Omichinski J.G., Sakaguchi K., Sakamoto H., Appella E., Gronenborn A.M., Clore G.M. The oligomerization domain of p53: crystal structure of the trigonal form. FEBS Lett. 1996, 399:166-170.
41. Milner J., Medcalf E.A. Cotranslation of activated mutant p53 with wild type drives the wild-type p53 protein into the mutant conformation. Cell 1991, 65:765-774.
42. Mittl P.R., Chene P., Grutter M.G. Crystallization and structure solution of p53 (residues 326-356) by molecular replacement using an NMR model as template. Acta Crystallograph. Sec D Biolog. Crystallogr. 1998, 54:86-89.
43. Olivier M., Eeles R., Hollstein M., Khan M.A., Harris C.C., Hainaut P. The IARC TP53 database: new online mutation analysis and recommendations to users. Hum. Mutat. 2002, 19:607-614.
44. Petitjean A., Mathe E., Kato S., Ishioka C., Tavtigian S.V., Hainaut P., Olivier M. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum. Mutat. 2007, 28:622-629.
45. Riley T., Sontag E., Chen P., Levine A. Transcriptional control of human p53-regulated genes. Nature reviews. Mole. Cell Biol. 2008, 9:402-412.
46. Rodriguez M.S., Desterro J.M., Lain S., Lane D.P., Hay R.T. Multiple C-terminal lysine residues target p53 for ubiquitin-proteasome-mediated degradation. Mol. Cell. Biol. 2000, 20:8458-8467.
47. Rodriguez M.S., Desterro J.M., Lain S., Midgley C.A., Lane D.P., Hay R.T. SUMO-1 modification activates the transcriptional response of p53. EMBO J. 1999, 18:6455-6461.
48. Rodriguez M.S., Wright J., Thompson J., Thomas D., Baleux F., Virelizier J.L., Hay R.T., Arenzana-Seisdedos F. Identification of lysine residues required for signal-induced ubiquitination and degradation of I kappa B-alpha in vivo. Oncogene 1996, 12:2425-2435.
49. Slee E.A., Zhu H., Chow S.C., MacFarlane M., Nicholson D.W., Cohen G.M. Benzyloxycarbonyl-Val-Ala-Asp (OMe) fluoromethylketone (Z-VAD.FMK) inhibits apoptosis by blocking the processing of CPP32. Biochem. J. 1996, 315(Pt. 1):21-24.
50. Soussi T., Beroud C. Assessing TP53 status in human tumours to evaluate clinical outcome. Nature reviews. Cancer 2001, 1:233-240.
51. Steinbrecher T., Latzer J., Case D.A. Revised AMBER parameters for bioorganic phosphates. J. Chem. Theory Comput. 2012, 8:4405-4412.
52. Sturzbecher H.W., Brain R., Addison C., Rudge K., Remm M., Grimaldi M., Keenan E., Jenkins J.R. A C-terminal alpha-helix plus basic region motif is the major structural determinant of p53 tetramerization. Oncogene 1992, 7:1513-1523.
53. Vogelstein B., Lane D., Levine A.J. Surfing the p53 network. Nature 2000, 408:307-310.
54. Zilfou J.T., Lowe S.W. Tumor suppressive functions of p53. Cold Spring Harbor Perspectives in Biology 2009, 1:a001883.