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p53 oligomerization status modulates cell fate decisions between growth, arrest and apoptosis

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Pages 3210-3219 | Received 18 Jul 2016, Accepted 21 Sep 2016, Published online: 04 Nov 2016

References

  • Chene P. The role of tetramerization in p53 function. Oncogene 2001; 20:2611-7; PMID:11420672; http://dx.doi.org/10.1038/sj.onc.1204373
  • Kitayner M, Rozenberg H, Kessler N, Rabinovich D, Shaulov L, Haran TE, Shakked Z. Structural basis of DNA recognition by p53 tetramers. Mol Cell 2006; 22:741-53; PMID:16793544; http://dx.doi.org/10.1016/j.molcel.2006.05.015
  • Bieging KT, Mello SS, Attardi LD. Unravelling mechanisms of p53-mediated tumour suppression. Nat Rev Cancer 2014; 14:359-70; PMID:24739573; http://dx.doi.org/10.1038/nrc3711
  • Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA, Butel JS, Bradley A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumors. Nature 1992; 356:215-21; PMID:1552940; http://dx.doi.org/10.1038/356215a0
  • Freed-Pastor WA, Prives C. Mutant p53: one name, many proteins. Genes Dev 2012; 26:1268-86; PMID:22713868; http://dx.doi.org/10.1101/gad.190678.112
  • Levine AJ, Oren M. The first 30 years of p53: growing ever more complex. Nat Rev Cancer 2009; 9:749-58; PMID:19776744; http://dx.doi.org/10.1038/nrc2723
  • Muller PA, Vousden KH. Mutant p53 in cancer: new functions and therapeutic opportunities. Cancer Cell 2014; 25:304-17; PMID:24651012; http://dx.doi.org/10.1016/j.ccr.2014.01.021
  • Kato S, Han SY, 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 USA 2003; 100:8424-9; PMID:12826609; http://dx.doi.org/10.1073/pnas.1431692100
  • 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; 24:6976-81; PMID:16007150; http://dx.doi.org/10.1038/sj.onc.1208839
  • Malkin D. Li-Fraumeni syndrome. Genes Cancer 2011; 2:475-84; PMID:21779515; http://dx.doi.org/10.1177/1947601911413466
  • Lomax ME, Barnes DM, Hupp TR, Picksley SM, Camplejohn RS. Characterization of p53 oligomerization domain mutations isolated from Li-Fraumeni and Li-Fraumeni like family members. Oncogene 1998; 17:643-9; PMID:9704930; http://dx.doi.org/10.1038/sj.onc.1201974
  • Warnock LJ, Knox A, Mee TR, Raines SA, Milner J. Influence of tetramerisation on site-specific post-translational modifications of p53: a comparison of human and murine p53 tumor suppressor protein. Cancer Biol Ther 2008; 7:1481-9; PMID:18769132; http://dx.doi.org/10.4161/cbt.7.9.6473
  • Itahana Y, Ke H, Zhang Y. p53 oligomerization is essential for its C-terminal lysine acetylation. J Biol Chem 2009; 284:5158-64; PMID:19106109; http://dx.doi.org/10.1074/jbc.M805696200
  • Lee IH, Kawai Y, Fergusson MM, Rovira II, Bishop AJ, Motoyama N, Cao L, Finkel T. Atg7 modulates p53 activity to regulate cell cycle and survival during metabolic stress. Science 2012; 336:225-8; PMID:22499945; http://dx.doi.org/10.1126/science.1218395
  • Ono W, Hayashi Y, Yokoyama W, Kuroda T, Kishimoto H, Ito I, Kimura K, Akaogi K, Waku T, Yanagisawa J. The nucleolar protein Myb-binding protein 1A (MYBBP1A) enhances p53 tetramerization and acetylation in response to nucleolar disruption. J Biol Chem 2014; 289:4928-40; PMID:24375404; http://dx.doi.org/10.1074/jbc.M113.474049
  • Meng X, Yue J, Liu Z, Shen Z. Abrogation of the transactivation activity of p53 by BCCIP down-regulation. J Biol Chem 2007; 282:1570-1576; PMID:17135243; http://dx.doi.org/10.1074/jbc.M607520200
  • Xu J, Zhou X, Wang J, Li Z, Kong X, Qian J, Hu Y, Fang JY. RhoGAPs attenuate cell proliferation by direct interaction with p53 tetramerization domain. Cell Rep 2013; 3:1526-38; PMID:23684608; http://dx.doi.org/10.1016/j.celrep.2013.04.017
  • Lui K, Sheikh MS, Huang Y. Regulation of p53 oligomerization by Ras superfamily protein RBEL1A. Genes Cancer 2015; 6:307-16; PMID:26413214
  • van Dieck J, Fernandez-Fernandez MR, Veprintsev DB, Fersht AR. Modulation of the oligomerization state of p53 by differential binding of proteins of the S100 family to p53 monomers and tetramers. J Biol Chem 2009; 284:13804-11; PMID:19297317; http://dx.doi.org/10.1074/jbc.M901351200
  • Foo RS, Nam YJ, Ostreicher MJ, Metzl MD, Whelan RS, Peng CF, Ashton AW, Fu W, Mani K, Chin SF, et al. Regulation of p53 tetramerization and nuclear export by ARC. Proc Natl Acad Sci USA 2007; 104:20826-31; PMID:18087040; http://dx.doi.org/10.1073/pnas.0710017104
  • Lee W, Harvey TS, Yin Y, Yau P, Litchfield D, Arrowsmith CH. Solution structure of the tetrameric minimum transforming domain of p53. Nat Struct Biol 1994; 1:877-90; PMID:7773777; http://dx.doi.org/10.1038/nsb1294-877
  • Jeffrey PD, Gorina S, Pavletich NP. Crystal structure of the tetramerization domain of the p53 tumor suppressor at 1.7 Å. Science 1995; 267:1498-502; PMID:7878469; http://dx.doi.org/10.1126/science.7878469
  • Nicholls CD, McClure KG, Shields MA, Lee PWK. Biogenesis of p53 involves cotranslational dimerization of monomers and posttranslational dimerization of dimers. J Biol Chem 2002; 277:12937-45; PMID:11805092; http://dx.doi.org/10.1074/jbc.M108815200
  • Weinberg RL, Veprintsev DB, Fersht AR. Cooperative binding of tetrameric p53 to DNA. J Mol Biol 2004; 341:1145-59; PMID:15321712; http://dx.doi.org/10.1016/j.jmb.2004.06.071
  • Ma L, Wagner J, Rice JJ, Hu W, Levine AJ, Stolovitzky GA. A plausible model for the digital response of p53 to DNA damage. Proc Natl Acad Sci USA 2005; 102:14266-71; PMID:16186499; http://dx.doi.org/10.1073/pnas.0501352102
  • Rajagopalan S, Huang F, Fersht AR. Single-molecule characterization of oligomerization kinetics and equilibria of the tumor suppressor p53. Nucleic Acids Res 2011; 29:2294-303; http://dx.doi.org/10.1093/nar/gkq800
  • Gaglia G, Guan Y, Shah JV, Lahav G. Activation and control of p53 tetramerization in individual living cells. Proc Natl Acad Sci USA 2013; 110:15497-501; PMID:24006363; http://dx.doi.org/10.1073/pnas.1311126110
  • Davison TS, Nie X, Ma W, Lin Y, Kay C, Benchimol S, Arrowsmith CH. Structure and functionality of a designed p53 dimer. J Mol Biol 2001; 307:605-17; PMID:11254385; http://dx.doi.org/10.1006/jmbi.2001.4450
  • Poon GM, Brokx RD, Sung M, Gariépy J. Tandem dimerization of the human p53 tetramerization domain stabilizes a primary dimer intermediate and dramatically enhances its oligomeric stability. J Mol Biol 2007; 365:1217-31; PMID:17113101; http://dx.doi.org/10.1016/j.jmb.2006.10.051
  • Brokx RD, Bolewska-Pedyczak E, Gariépy J. A stable human p53 heterotetramer based on constructive charge interactions within the tetramerization domain. J Biol Chem 2003; 278:2327-32; PMID:12433927; http://dx.doi.org/10.1074/jbc.M208528200
  • Lang V, Pallara C, Zabala A, Lobato-Gil S, Lopitz-Otsoa F, Farrás R, Hjerpe R, Torres-Ramos M, Zabaleta L, Blattner C, et al. Tetramerization-defects of p53 result in aberrant ubiquitylation and transcriptional activity. Mol Oncol 2014; 8:1026-42; PMID:24816189; http://dx.doi.org/10.1016/j.molonc.2014.04.002
  • Timofeev O, Schlereth K, Wanzel M, Braun A, Nieswandt B, Pagenstecher A, Rosenwald A, Elsässer HP, Stiewe T. p53 DNA binding cooperativity is essential for apoptosis and tumor suppression in vivo. Cell Rep 2013; 30:1512-25; http://dx.doi.org/10.1016/j.celrep.2013.04.008
  • Li T, Kon N, Tan M, Ludwig T, Zhao Y, Baer R, Wei G. Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell 2012; 149:1269-83; PMID:22682249; http://dx.doi.org/10.1016/j.cell.2012.04.026
  • Igarashi H, Hirano H, Yahagi A, Saika T, Ishihara K. Anti-apoptotic roles for the mutant p53R248Q through suppression of p53-regulated apoptosis-inducing protein 1 in the RA-derived fibroblast-like synoviocyte cell line MH7A. Clin Immunol 2014; 150:12-21; PMID:24316591; http://dx.doi.org/10.1016/j.clim.2013.10.013
  • Phang BH, Othman R, Bougeard G, Chia RH, Frebourg T, Tang CL, Cheah PY, Sabapathy K. Amino-terminal p53 mutations lead to expression of apoptosis proficient p47 and prognosticate better survival, but predispose to tumorigenesis. Proc Natl Acad Sci USA 2015; 112:E6349-58; PMID:26578795; http://dx.doi.org/10.1073/pnas.1510043112
  • Beckerman R, Yoh K, Mattia-Sansobrino M, Zupnick A, Laptenko O, Karni-Schmidt O, Ahn J, Byeon I, Keezer S, Prives C. Lysines in the tetramerization domain of p53 selectively modulate G1 arrest. Cell Cycle 2016; 15:1425-38; PMID:27210019; http://dx.doi.org/10.1080/15384101.2016.1170270
  • Khoo KH, Verma CS, Lane DP. Drugging the p53 pathway: understanding the route to clinical efficacy. Nat Rev Drug Discov 2014; 13:217-36; PMID:24577402; http://dx.doi.org/10.1038/nrd4288
  • Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T, Nishimori H, Tamai K, Tikino T, Nakamaru Y, et al. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by ser-46 phosphorylated p53. Cell 2000; 102:849-62; PMID:11030628; http://dx.doi.org/10.1016/S0092-8674(00)00073-8
  • Zhang XP, Liu F, Cheng Z, Wang W. Cell fate decision mediated by p53 pulses. Proc Natl Acad Sci USA 2009; 106:12245-50; PMID:19617533; http://dx.doi.org/10.1073/pnas.0813088106
  • Chen X, Chen J, Gan S, Guan G, Zhou Y, Ouyang Q, Shi J. DNA damage strength modulates a bimodal switch of p53 dynamics for cell-fate control. BMC Biol 2013; 11:73; PMID:23800173; http://dx.doi.org/10.1186/1741-7007-11-73
  • Zhang XP, Liu F, Wang W. Two-phase dynamics of p53 in the DNA damage response. Proc Natl Acad Sci USA 2011; 108:8990-5; PMID:21576488; http://dx.doi.org/10.1073/pnas.1100600108
  • Matsuda K, Yoshida K, Taya Y, Nakamura K, Nakamura Y, Arakawa H. p53AIP1 regulates the mitochondrial apoptotic pathway. Cancer Res 2002; 62:2883-9; PMID:12019168
  • El-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell 1993; 75:817-25; PMID:8242752; http://dx.doi.org/10.1016/0092-8674(93)90500-P
  • Waldman T, Kinzler KW, Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res 1995; 55:5187-90; PMID:7585571

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