Structural convergence of unstructured p53 family transactivation domains in mdm2 recognition

Cell Cycle

Volumn 14, Issue 4, 2015, Pages 533-543

  Jae Sun, Shin ^a   Ji Hyang, Ha ^a   Dong Hwa, Lee ^a   Kyoung Seok, Ryu ^b   Kwang Hee, Bae ^a   Byoung, Chul Park ^a   Sung, Goo Park ^a   Gwan Su, Yi ^c   Seung Wook, Chi ^a  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Korea Basic Science Institute (KBSI)   (South Korea)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

Complex structure; MDM2; NMR; P53 family; P73; Transactivation domain

Indexed keywords

PROTEIN MDM2; PROTEIN P53; PROTEIN P63; PROTEIN P73; DNA BINDING PROTEIN; MDM2 PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; NUCLEAR PROTEIN; PROTEIN BINDING; TP63 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN P73;

ARTICLE; BINDING AFFINITY; CANCER INHIBITION; CIRCULAR DICHROISM; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR MIMICRY; MOLECULAR RECOGNITION; MUTAGENESIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TRANSACTIVATION; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; GENE STRUCTURE; GENETICS; HUMAN; MOLECULAR GENETICS; TRANSCRIPTION INITIATION;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; DNA-BINDING PROTEINS; GENE COMPONENTS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTO-ONCOGENE PROTEINS C-MDM2; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 84923328581     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.1080/15384101.2014.998056     Document Type: Article

References (46)

1. Jost CA, Marin MC, Kaelin WG, Jr. p73 is a simian [correction of human] p53-related protein that can induce apoptosis. Nature 1997; 389:191-4; PMID:9296498
2. Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dotsch V, Andrews NC, Caput D, McKeon F. p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominantnegative activities. Mol Cell 1998; 2:305-16; PMID:9774969
3. Mills AA, Zheng B,Wang XJ, VogelH, Roop DR, Bradley A. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 1999; 398:708-13; PMID:10227293; http://dx.doi.org/10.1038/19531
4. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, Tabin C, Sharpe A, Caput D, Crum C, et al. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 1999; 398:714-8; PMID:10227294; http://dx.doi.org/ 10.1038/19539
5. Yang A, Walker N, Bronson R, Kaghad M, Oosterwegel M, Bonnin J, Vagner C, Bonnet H, Dikkes P, Sharpe A, et al. p73-deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours. Nature 2000; 404:99-103; PMID:10716451; http://dx. doi.org/10.1038/35003607
6. Danilova N, SakamotoKM, Lin S. p53 family in development. Mech Dev 2008; 125:919-31; PMID:18835440; http://dx.doi.org/10.1016/j.mod.2008.09.003
7. Momand J, Zambetti GP, Olson DC, George D, Levine AJ. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 1992; 69:1237-45; PMID:1535557; http://dx.doi.org/10.1016/0092-8674(92)90644-R
8. Oliner JD, Pietenpol JA, Thiagalingam S, Gyuris J, Kinzler KW, Vogelstein B. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 1993; 362:857-60; PMID:8479525; http://dx. doi.org/10.1038/362857a0
9. Balint E, Bates S, Vousden KH. Mdm2 binds p73 alpha without targeting degradation. Oncogene 1999; 18:3923-9; PMID:10435614; http://dx.doi.org/ 10.1038/sj.onc.1202781
10. Zeng X, Chen L, Jost CA, Maya R, Keller D, Wang X, Kaelin WG, Jr., Oren M, Chen J, Lu H. MDM2 suppresses p73 function without promoting p73 degradation. Mol Cell Biol 1999; 19:3257-66; PMID:10207051
11. Kadakia M, Slader C, Berberich SJ. Regulation of p63 function by Mdm2 and MdmX. DNA Cell Biol 2001; 20:321-30; PMID:11445003; http://dx.doi.org/ 10.1089/10445490152122433
12. Zdzalik M, Pustelny K, Kedracka-Krok S, Huben K, Pecak A, Wladyka B, Jankowski S, Dubin A, Potempa J, Dubin G. Interaction of regulators Mdm2 and Mdmx with transcription factors p53, p63 and p73. Cell Cycle 2010; 9:4584-91; PMID:21088494; http:// dx.doi.org/10.4161/cc.9.22.13871
13. Kubbutat MH, Jones SN, Vousden KH. Regulation of p53 stability by Mdm2. Nature 1997; 387:299-303; PMID:9153396; http://dx.doi.org/10.1038/387299a0
14. Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997; 387:296-9; PMID:9153395; http://dx.doi.org/10.1038/387296a0
15. Okamoto K, Taya Y, Nakagama H. Mdmx enhances p53 ubiquitination by altering the substrate preference of the Mdm2 ubiquitin ligase. FEBS Lett 2009; 583:2710-4; PMID:19619542; http://dx.doi.org/ 10.1016/j.febslet.2009.07.021
16. Danovi D, Meulmeester E, Pasini D, Migliorini D, Capra M, Frenk R, de Graaf P, Francoz S, Gasparini P, Gobbi A, et al. Amplification of Mdmx (or Mdm4) directly contributes to tumor formation by inhibiting p53 tumor suppressor activity. Mol Cell Biol 2004; 24:5835-43; PMID:15199139; http://dx.doi.org/ 10.1128/MCB.24.13.5835-5843.2004
17. 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 and Differ 2008; 15:841-8; PMID:18219319; http://dx.doi.org/ 10.1038/sj.cdd.4402309
18. Brown CJ, Lain S, Verma CS, Fersht AR, Lane DP. Awakening guardian angels: drugging the p53 pathway. Nature Rev Cancer 2009; 9:862-73; PMID:19935675; http://dx.doi.org/10.1038/nrc2763
19. Ventura A, Kirsch DG, McLaughlin ME, Tuveson DA, Grimm J, Lintault L, Newman J, Reczek EE, Weissleder R, Jacks T. Restoration of p53 function leads to tumour regression in vivo. Nature 2007; 445:661-5; PMID:17251932; http://dx.doi.org/10.1038/nature 05541
20. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, Cordon-Cardo C, Lowe SW. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007; 445:656-60; PMID:17251933; http://dx.doi.org/ 10.1038/nature05529
21. Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science 1991; 253:49-53; PMID:1905840; http://dx.doi.org/ 10.1126/science.1905840
22. Melino G, De Laurenzi V, Vousden KH. p73: Friend or foe in tumorigenesis. Nature Rev Cancer 2002; 2:605-15; PMID:12154353; http://dx.doi.org/ 10.1038/nrc861
23. Zawacka-Pankau J, Kostecka A, Sznarkowska A, Hedstrom E, Kawiak A. p73 tumor suppressor protein: a close relative of p53 not only in structure but also in anti-cancer approach? Cell Cycle 2010; 9:720-8; PMID:20160513; http://dx.doi.org/10.4161/cc.9.4. 10668
24. Vayssade M, Haddada H, Faridoni-Laurens L, Tourpin S, Valent A, Benard J, Ahomadegbe JC. P73 functionally replaces p53 in Adriamycin-treated, p53-deficient breast cancer cells. Int J Cancer 2005; 116:860-9; PMID:15849742; http://dx.doi.org/10.1002/ijc.21033
25. Schon O, Friedler A, Bycroft M, Freund SM, Fersht AR. Molecular mechanism of the interaction between MDM2 and p53. J Mol Biol 2002; 323:491-501; PMID:12381304; http://dx.doi.org/10.1016/S0022-2836(02)00852-5
26. Kussie PH, Gorina S, Marechal V, Elenbaas B, Moreau J, Levine AJ, Pavletich NP. Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 1996; 274:948-53; PMID:8875929; http://dx.doi.org/10.1126/science. 274.5289.948
27. Picksley SM, Vojtesek B, Sparks A, Lane DP. Immunochemical analysis of the interaction of p53 with MDM2;-fine mapping of the MDM2 binding site on p53 using synthetic peptides. Oncogene 1994; 9:2523-9; PMID:8058315
28. McCoy MA, Gesell JJ, Senior MM, Wyss DF. Flexible lid to the p53-binding domain of human Mdm2: implications for p53 regulation. Proc Natl Acad Sci USA 2003; 100:1645-8; PMID:12552135
29. Uhrinova S, Uhrin D, Powers H, Watt K, Zheleva D, Fischer P, McInnes C, Barlow PN. Structure of free MDM2 N-terminal domain reveals conformational adjustments that accompany p53-binding. J Mol Biol 2005; 350:587-98; PMID:15953616; http://dx.doi. org/10.1016/j.jmb.2005.05.010
30. Showalter SA, Bruschweiler-Li L, Johnson E, Zhang F, Bruschweiler R. Quantitative lid dynamics of MDM2 reveals differential ligand binding modes of the p53-binding cleft. J Am Chem Soc 2008; 130:6472-8; PMID:18435534; http://dx.doi.org/10.1021/ja800201j
31. Mavinahalli JN, Madhumalar A, Beuerman RW, Lane DP, Verma C. Differences in the transactivation domains of p53 family members: a computational study. BMC Genomics 2010; 11 Suppl 1:S5; PMID:20158876
32. Uesugi M, Nyanguile O, Lu H, Levine AJ, Verdine GL. Induced alpha helix in the VP16 activation domain upon binding to a human TAF. Science 1997; 277:1310-3; PMID:9271577; http://dx.doi.org/ 10.1126/science.277.5330.1310
33. Zor T, De Guzman RN, Dyson HJ, Wright PE. Solution structure of the KIX domain of CBP bound to the transactivation domain of c-Myb. J Mol Biol 2004; 337:521-34; PMID:15019774; http://dx.doi.org/ 10.1016/j.jmb.2004.01.038
34. Ha JH, Shin JS, Yoon MK, Lee MS, He F, Bae KH, Yoon HS, Lee CK, Park SG, Muto Y, et al. Dual-site interactions of p53 protein transactivation domain with anti-apoptotic Bcl-2 family proteins reveal a highly convergent mechanism of divergent p53 pathways. J Biol Chem 2013; 288:7387-98; PMID:23316052; http://dx.doi.org/10.1074/jbc.M112.400754
35. Ha JH, Won EY, Shin JS, Jang M, Ryu KS, Bae KH, Park SG, Park BC, Yoon HS, Chi SW. Molecular mimicry-based repositioning of nutlin-3 to anti-apoptotic Bcl-2 family proteins. J Am Chem Soc 2011; 133:1244-7; PMID:21210687; http://dx.doi.org/ 10.1021/ja109521f
36. Bochkareva E, Kaustov L, Ayed A, Yi GS, Lu Y, Pineda-Lucena A, Liao JC, Okorokov AL, Milner J, Arrowsmith CH, et al. Single-stranded DNA mimicry in the p53 transactivation domain interaction with replication protein A. Proc Natl Acad Sci USA 2005; 102:15412-7.
37. Teufel DP, Bycroft M, Fersht AR. Regulation by phosphorylation of the relative affinities of the N-terminal transactivation domains of p53 for p300 domains and Mdm2. Oncogene 2009; 28:2112-8; PMID:19363523; http://dx.doi.org/10.1038/onc.2009.71
38. Burge S, Teufel DP, Townsley FM, Freund SM, Bycroft M, Fersht AR. Molecular basis of the interactions between the p73 N terminus and p300: effects on transactivation and modulation by phosphorylation. Proc Natl Acad Sci USA 2009; 106:3142-7.
39. ZhengT,Wang J,Chen X, Meng X, Song X, Lu Z, Jiang H, Liu L. Disruption of p73-MDM2 binding synergizes with gemcitabine to induce apoptosis in HuCCT1 cholangiocarcinoma cell line with p53 mutation. Tumour Biol 2010; 31:287-95; PMID:20422343; http://dx.doi. org/10.1007/s13277-010-0035-7
40. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 1995; 6:277-93; PMID:8520220; http://dx.doi.org/ 10.1007/BF00197809
41. Herrmann T, Guntert P, Wuthrich K. Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J Biomol NMR 2002; 24:171-89; PMID:12522306; http://dx.doi.org/10.1023/ A:1021614115432
42. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM. The Xplor-NIH NMR molecular structure determination package. J Magn Reson 2003; 160:65-73; PMID:12565051; http://dx.doi.org/10.1016/S1090-7807(02)00014-9
43. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM. AQUA and PROCHECKNMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 1996; 8:477-86; PMID:9008363; http://dx.doi.org/10.1007/ BF00228148
44. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB, 3rd, Snoeyink J, Richardson JS, et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids.Nucleic Acids Res 2007; 35:W375-83; PMID:17452350; http:// dx.doi.org/10.1093/nar/gkm216
45. Dominguez C, Boelens R, Bonvin AM. HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 2003; 125:1731-7; PMID:12580598; http://dx.doi.org/ 10.1021/ja026939x
46. Fernandez-Recio J, Totrov M, Abagyan R. Identification of protein-protein interaction sites from docking energy landscapes. J Mol Biol 2004; 335:843-65; PMID:14687579; http://dx.doi.org/10.1016/j.jmb. 2003.10.069