P53 at the crossroads between cancer and neurodegeneration

Free Radical Biology and Medicine

Volumn 52, Issue 9, 2012, Pages 1727-1733

  Lanni, Cristina ^a   Racchi, Marco ^a   Memo, Maurizio ^b   Govoni, Stefano ^a   Uberti, Daniela ^b  

^a UNIVERSITY OF PAVIA   (Italy)

^b UNIVERSITY OF BRESCIA   (Italy)

Author keywords

Alzheimer disease; Cancer; Conformational alteration; Free radicals; Gain of function; Oxidative stress; p53

Indexed keywords

PROTEIN P53;

AGING; ALZHEIMER DISEASE; APOPTOSIS; CELL AGING; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL DEATH; CELL FATE; CELL SURVIVAL; CELLULAR STRESS RESPONSE; DEGENERATIVE DISEASE; DNA DAMAGE; DNA REPAIR; DNA SEQUENCE; GENE MUTATION; GENOTOXICITY; HUMAN; LOSS OF FUNCTION MUTATION; NEOPLASM; NERVE CELL; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DNA INTERACTION; PROTEIN FOLDING; PROTEIN FUNCTION; REVIEW; SENESCENCE; SIGNAL TRANSDUCTION; TRANSACTIVATION;

GENES, P53; HUMANS; MUTATION; NEOPLASMS; NEURODEGENERATIVE DISEASES;

EID: 84858970616     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.02.034     Document Type: Review

References (124)

1. P.A. Jones, and S.B. Baylin The epigenomics of cancer Cell 128 2007 683 692
2. M. Esteller Epigenetics in cancer N. Engl. J. Med. 358 2008 1148 1159
3. M. Esteller Relevance of DNA methylation in the management of cancer Lancet Oncol. 4 2003 351 358
4. A.P. Feinberg, and B. Vogelstein Hypomethylation distinguishes genes of some human cancers from their normal counterparts Nature 301 1983 89 92
5. H. Tohgi, K. Utsugisawa, Y. Nagane, M. Yoshimura, Y. Genda, and M. Ukitsu Reduction with age in methylcytosine in the promoter region - 224 ~ - 101 of the amyloid precursor protein gene in autopsy human cortex Brain Res. Mol. Brain Res. 70 1999 288 292
6. R.L. West, J.M. Lee, and L.E. Maroun Hypomethylation of the amyloid precursor protein gene in the brain of an Alzheimer's disease patient J. Mol. Neurosci. 6 1995 141 146
7. N. Iwata, S. Tsubuki, Y. Takaki, K. Watanabe, M. Sekiguchi, E. Hosoki, M. Kawashima-Morishima, H.J. Lee, E. Hama, Y. Sekine-Aizawa, and T.C. Saido Identification of the major Aβ1-42-degrading catabolic pathway in brain parenchyma: suppression leads to biochemical and pathological deposition Nat. Med. 6 2000 143 150
8. K.L. Chen, S.S. Wang, Y.Y. Yang, R.Y. Yuan, R.M. Chen, and C.J. Hu The epigenetic effects of amyloid-β(1-40) on global DNA and neprilysin genes in murine cerebral endothelial cells Biochem. Biophys. Res. Commun. 378 2009 57 61
9. K.D. Siegmund, C.M. Connor, M. Campan, T.I. Long, D.J. Weisenberger, D. Biniszkiewicz, R. Jaenisch, P.W. Laird, and S. Akbarian DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons PLoS One 2 2007 e895
10. R.S. Jope, C.J. Yuskaitis, and E. Beurel Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics Neurochem. Res. 32 2007 577 595
11. K.P. Lu, and X.Z. Zhou The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signaling and disease Nat. Rev. Mol. Cell Biol. 8 2007 904 916
12. T. Li, H. Wen, C. Brayton, F.M. Laird, G. Ma, S. Peng, L. Placanica, T.C. Wu, B.J. Crain, D.L. Price, C.G. Eberhart, and P.C. Wong Moderate reduction of γ-secretase attenuates amyloid burden and limits mechanism-based liabilities J. Neurosci. 27 2007 10849 10859
13. C.M. Roe, M.I. Behrens, C. Xiong, J.P. Miller, and J.C. Morris Alzheimer disease and cancer Neurology 64 2005 895 898
14. C.M. Roe, A.L. Fitzpatrick, C. Xiong, W. Sieh, L. Kuller, J.P. Miller, M.M. Williams, R. Kopan, M.I. Behrens, and J.C. Morris Cancer linked to Alzheimer disease but not vascular dementia Neurology 74 2010 106 112
15. L.H. Heflin, B.E. Meyerowitz, P. Hall, P. Lichtenstein, B. Johansson, N.L. Pedersen, and M. Gatz Cancer as a risk factor for long-term cognitive deficits and dementia J. Natl. Cancer Inst. 97 2005 854 856
16. J.S. Nelson Alzheimer pathology in elderly patients with glioblastoma multiforme Arch. Pathol. Lab. Med. 126 2002 1515 1517
17. S. Francisconi, M. Codenotti, G. Ferrari-Toninelli, D. Uberti, and M. Memo Preservation of DNA integrity and neuronal degeneration Brain Res. Brain Res. Rev. 48 2005 347 351
18. A. Copani, D. Uberti, M.A. Sortino, V. Bruno, F. Nicoletti, and M. Memo Activation of cell-cycle-associated proteins in neuronal death: a mandatory or dispensable path? Trends Neurosci. 24 2001 25 31
19. J. Campisi Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors Cell 120 2005 513 522
20. Y. Yang, D.S. Geldmacher, and K. Herrup DNA replication precedes neuronal cell death in Alzheimer's disease J. Neurosci. 21 2001 2661 2668
21. A.J. Levine p53, the cellular gatekeeper for growth and division Cell 88 1997 323 331
22. C. Méplan, M.J. Richard, and P. Hainaut Redox signalling and transition metals in the control of the p53 pathway Biochem. Pharmacol. 59 2000 25 33
23. C.L. Brooks, and W. Gu Ubiquitination, phosphorylation and acetylation: the molecular basis for p53 regulation Curr. Opin. Cell Biol. 15 2003 164 171
24. S. Di Giovanni, C.D. Knights, M. Rao, A. Yakovlev, J. Beers, J. Catania, M.L. Avantaggiati, and A.I. Faden The cancer suppressor protein p53 is required for neurite outgrowth and axon regeneration EMBO J. 25 2006 4084 4096
25. C.D. Knights, J. Catania, S. Di Giovanni, S. Muratoglu, R. Perez, A. Swartzbeck, A.A. Quong, X. Zhang, T. Beerman, R.G. Pestell, and M.L. Avantaggiati Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate J. Cell Biol. 173 2006 533 544
26. B. Vogelstein, D. Lane, and A.J. Levine Surfing the p53 network Nature 408 2000 307 310
27. C.J. Bakkenist, and M.B. Kastan Initiating cellular stress responses Cell 118 2004 9 17
28. S.T. Al Rashid, G. Dellaire, A. Cuddihy, F. Jalali, M. Vaid, C. Coackley, M. Folkard, Y. Xu, B.P. Chen, D.J. Chen, L. Lilge, K.M. Prise, D.P. Bazett Jones, and R.G. Bristow Evidence for the direct binding of phosphorylated p53 to sites of DNA breaks in vivo Cancer Res. 65 2005 10810 10821
29. C. Guillouf, X. Graña, M. Selvakumaran, A. De Luca, A. Giordano, B. Hoffman, and D.A. Liebermann Dissection of the genetic programs of p53-mediated G1 growth arrest and apoptosis: blocking p53-induced apoptosis unmasks G1 arrest Blood 85 1995 2691 2698
30. F. Rodier, J. Campisi, and D. Bhaumik Two faces of p53: aging and cancer suppression Nucleic Acids Res. 35 2007 7475 7484
31. E. Meulmeester, and A.G. Jochemsen p53: a guide to apoptosis Curr. Cancer Drug Targets 8 2008 87 97
32. M. Shawi, and C. Autexier Telomerase, senescence and ageing Mech. Ageing Dev. 129 2008 3 10
33. L.A. Donehower Does p53 affect organismal aging? J. Cell. Physiol. 192 2002 23 33
34. A. Sigal, and V. Rotter Oncogenic mutations of the p53 cancer suppressor: the demons of the guardian of the genome Cancer Res. 60 2000 6788 6793
35. A. Zalcenstein, P. Stambolsky, L. Weisz, M. Müller, D. Wallach, T.M. Goncharov, P.H. Krammer, V. Rotter, and M. Oren Mutant p53 gain of function: repression of CD95(Fas/APO-1) gene expression by cancer-associated p53 mutants Oncogene 22 2003 5667 5676
36. E. Kim, and W. Deppert Transcriptional activities of mutant p53: when mutations are more than a loss J. Cell. Biochem. 93 2004 878 886
37. R. Brosh, and V. Rotter When mutants gain new powers: news from the mutant p53 field Nat. Rev. Cancer 9 2009 701 713
38. K.B. Wong, B.S. DeDecker, S.M.V. Freund, M.R. Proctor, M. Bycroft, and A.R. Fersht Hot spot mutants of p53 core domain evince characteristic local structural changes Proc. Natl. Acad. Sci. U. S. A. 96 1999 8438 8442
39. Y. Cho, S. Gorina, P.D. Jeffrey, and N.P. Pavletich Crystal structure of a p53 cancer suppressor-DNA complex: understanding cancerigenic mutations Science 265 1994 346 355
40. A. Gualberto, K. Aldape, K. Kozakiewicz, and T.D. Tlsy An oncogenic form of p53 confers a dominant, gain of function phenotype that disrupts spindle checkpoint control Proc. Natl. Acad. Sci. U. S. A. 95 1998 5166 5171
41. R. Li, P.D. Suthpin, D. Schwarz, D. Matas, N. Almong, R. Wolkowicz, N. Goldfinger, H. Pei, M. Prokocimer, and V. Rotter Mutant p53 protein expression interferes with p53-independent apoptotic pathway Oncogene 16 1998 3269 3277
42. G. Blandino, A.J. Levine, and M. Oren Mutant p53 gain of function: differential effects of different p53 mutants on resistance of cultured cells on chemotherapy Oncogene 18 1999 477 485
43. T. Aas, A.L. Borrensen, S. Geisler, B. Smith-Sorensen, H. Johnsen, J. Varhaug, L.A. Akslen, and P.E. Lonning Specific p53 mutations are associated with de novo resistance to doxorubicin in breast cancer patients Nat. Med. 2 1996 811 814
44. E.M. Berns, J.A. Foekens, R. Vossen, M.P. Look, P. Devilee, S.C. Henzen-Logmans, I.L. van Staveren, W.L. van Putten, M. Inganäs, M.E. Meijer-van Gelder, C. Cornelisse, C.J. Claassen, H. Portengen, B. Bakker, and J.G. Klijn Complete sequencing of TP53 predicts poor response to systemic therapy of advanced breast cancer Cancer Res. 60 2000 2155 2162
45. S. Geisler, A.L. Borrensen-Dale, H. Johnsen, T. Aas, J. Geisler, L.A. Akslen, G. Anker, and P.E. Lonning TP53 gene mutations predict the response to neoadjuvant treatment with 5-fluorouracil and mitomycin in locally advanced breast cancer Clin. Cancer Res. 9 2003 5582 5588
46. M.J. Scian, K.E. Stagliano, M.A. Ellis, S. Hassan, M. Bowman, M.F. Miles, S.P. Deb, and S. Deb Modulation of gene expression by cancer-derived p53 mutants Cancer Res. 64 2004 7447 7454
47. T.J. O'Farrell, P. Ghosh, N. Dobashi, C.Y. Sasaki, and D.L. Longo Comparison of the effect of mutant and wild-type p53 on global gene expression Cancer Res. 64 2004 8199 8207
48. L. Weisz, A. Zalcenstein, P. Stambolsky, Y. Cohen, N. Goldfinger, M. Oren, and V. Rotter Transactivation of EGR1 gene contributes to mutant p53 gain of function Cancer Res. 64 2004 8318 8327
49. G.A. Lang, T. Iwakuma, Y.A. Suh, G. Liu, V.A. Rao, J.M. Parant, Y.A. Valentin-Vega, T. Terzian, L.C. Caldwell, L.C. Strong, A.K. El-Naggar, and G. Lozano Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome Cell 119 2004 861 872
50. C. Gaiddon, M. Lokshin, J. Ahn, T. Zhang, and C. Prives A subset of cancer derived mutant forms of p53 down regulate p63 and p73 through a direct interaction with the p53 core domain Mol. Cell. Biol. 21 2001 1874 1887
51. S. Strano, S. Dell'Orso, S. Di Agostino, G. Fontemaggi, A. Sacchi, and G. Blandino Mutant p53: an oncogenic transcription factor Oncogene 26 2007 2212 2219
52. K.M. Webley, A.J. Shorthouse, and J.A. Royds Effect of mutation and conformation on the function of p53 in colorectal cancer J. Pathol. 191 2000 361 367
53. H.H. Wu, J.A. Thomas, and J. Momand p53 protein oxidation in cultured cells in response to pyrrolidine dithiocarbamate: a novel method for relating the amount of p53 oxidation in vivo to the regulation of p53-responsive genes Biochem. J. 351 2000 87 93
54. P. Hainaut, and J. Milner Redox modulation of p53 conformation and sequence-specific DNA binding in vitro Cancer Res. 53 1993 4469 4473
55. S. Calmels, P. Hainaut, and H. Ohshima Nitric oxide induces conformational and functional modifications of wild-type p53 tumor suppressor protein Cancer Res. 57 1997 3365 3369
56. D. Parks, R. Bolinger, and K. Mann Redox state regulates binding of p53 to sequence-specific DNA, but not to non-specific or mismatched DNA Nucleic Acids Res. 25 1997 1289 1295
57. G.Y. Liou, and P. Storz Reactive oxygen species in cancer Free. Radic. Res. 44 2010 479 496
58. J. Blumberg Use of biomarkers of oxidative stress in research studies J. Nutr. 134 2004 3188S 3189S
59. M. Reth Hydrogen peroxide as second messenger in lymphocyte activation Nat. Immunol. 3 2002 1129 1134
60. H. Liu, R. Colavitti, I.I. Rovira, and T. Finkel Redox-dependent transcriptional regulation Circ. Res. 97 2005 967 974
61. Y. Kabe, K. Ando, S. Hirao, M. Yoshida, and H. Handa Redox regulation of NF-κB activation: distinct redox regulation between the cytoplasm and the nucleus Antioxid. Redox Signal. 7 2005 395 403
62. M. Ishikawa, S. Numazawa, and T. Yoshida Redox regulation of the transcriptional repressor Bach1 Free Radic. Biol. Med. 38 2005 1344 1352
63. D. Uberti, C. Lanni, T. Carsana, S. Francisconi, C. Missale, M. Racchi, S. Govoni, and M. Memo Identification of a mutant-like conformation of p53 in fibroblasts from sporadic Alzheimer's disease patients Neurobiol. Aging 27 2006 1193 1201
64. G. Achanta, and P. Huang Role of p53 in sensing oxidative DNA damage in response to reactive oxygen species-generating agents Cancer Res. 64 2004 6233 6239
65. A. Wiseman p53 protein or BID protein select the route to either apoptosis (programmed cell death) or to cell cycle arrest opposing carcinogenesis after DNA damage by ROS Med. Hypotheses 67 2006 296 299
66. P. Hainaut, and K. Mann Zinc binding and redox control of p53 structure and function Antioxid. Redox Signal. 3 2001 611 623
67. R. Rainwater, D. Parks, M.E. Anderson, P. Tegtmeyer, and K. Mann Role of cysteine residues in regulation of p53 function Mol. Cell. Biol. 15 1995 3892 3903
68. S. Salvioli, M. Capri, L. Bucci, C. Lanni, M. Racchi, D. Uberti, M. Memo, D. Mari, S. Govoni, and C. Franceschi Why do centenarians escape or postpone cancer? The role of IGF-1, inflammation and p53 Cancer Immunol. Immunother. 58 2009 1909 1917
69. W. Chatoo, M. Abdouh, and G. Bernier p53 pro-oxidant activity in the central nervous system: implication in aging and neurodegenerative diseases Antioxid. Redox Signal. 15 2011 1729 1737
70. H. Hafsi, and P. Hainaut Redox control and interplay between p53 isoforms: roles in the regulation of basal p53 levels, cell fate, and senescence Antioxid. Redox Signal. 15 2011 1655 1667
71. A. Salminen, and K. Kaarniranta Control of p53 and NF-κB signaling by WIP1 and MIF: role in cellular senescence and organismal aging Cell. Signal. 23 2011 747 752
72. A. Salminen, J. Ojala, and K. Kaarniranta Apoptosis and aging: increased resistance to apoptosis enhances the aging process Cell. Mol. Life Sci. 68 2011 1021 1031
73. R.E. Castro, M.M. Santos, P.M. Glória, C.J. Ribeiro, D.M. Ferreira, J.M. Xavier, R. Moreira, and C.M. Rodrigues Cell death targets and potential modulators in Alzheimer's disease Curr. Pharm. Des. 16 2010 2851 2864
74. C. Lanni, M. Racchi, D. Uberti, G. Mazzini, S. Stanga, E. Sinforiani, M. Memo, and S. Govoni Pharmacogenetics and pharmacogenomics, trends in normal and pathological ageing studies: focus on p53 Curr. Pharm. Des. 14 2008 2665 2671
75. C. Alves da Costa, and F. Checler Apoptosis in Parkinson's disease: is p53 the missing link between genetic and sporadic Parkinsonism? Cell. Signal. 23 2011 963 968
76. S. Ranganathan, and R. Bowser p53 and cell cycle proteins participate in spinal motor neuron cell death in ALS Open Pathol. J. 4 2010 11 22
77. S.D. Tyner, S. Venkatachalam, J. Choi, S. Jones, N. Ghebranious, H. Igelmann, X. Lu, G. Soron, B. Cooper, B. Cooper, C. Brayton, S. Hee Park, T. Thompson, G. Karsenty, A. Bradley, and L.A. Donehower p53 mutant mice that display early ageing-associated phenotypes Nature 415 2002 45 53
78. M. Dumble, L. Moore, S.M. Chambers, H. Geiger, G. Van Zant, M.A. Goodell, and L.A. Donehower The impact of altered p53 dosage on hematopoietic stem cell dynamics during aging Blood 109 2007 1736 1742
79. B. Maier, W. Gluba, B. Bernier, T. Turner, H. Mohammad, T. Guise, A. Sutherland, M. Thorner, and H. Scrable Modulation of mammalian life span by the short isoform of p53 Genes Dev. 18 2004 306 319
80. V.L. Bukhman, N.N. Ninkina, P.M. Chumakov, M.A. Khilenkova, and O.P. Samarina Structural organization of the human p53 gene. I. Molecular cloning of the human p53 gene Genetika 23 1987 1547 1554
81. D. Van Heemst, S.P. Mooijaart, M. Beekman, J. Schreuder, A.J. De Craen, B.W. Brandt, P.E. Slagboom, and R.G. Westendorp Variation in the human TP53 gene affects old age survival and cancer mortality Exp. Gerontol. 40 2005 11 15
82. E. Mammano, C. Belluco, M. Bonafé, F. Olivieri, E. Mugianesi, C. Barbi, M. Mishto, M. Cosci, C. Franceschi, M. Lise, and D. Nitti Association of p53 polymorphisms and colorectal cancer: modulation of risk and progression Eur. J. Surg. Oncol. 35 2009 415 419
83. A. Ander Matheu, A. Maraver, P. Klatt, I. Flores, I. Garcia-Cao, C. Borras, J.M. Flores, J. Viña, M.A. Blasco, and M. Serrano Delayed ageing through damage protection by the Arf/p53 pathway Nature 448 2007 375 379
84. Z. Feng, W. Hu, A.K. Teresky, E. Hernando, C. Cordon-Cardo, and A.J. Levine Declining p53 function in the aging process: a possible mechanism for the increased cancer incidence in older populations Proc. Natl. Acad. Sci. U. S. A. 104 2007 16633 16638
85. A. Seluanov, V. Gorbunova, A. Falcovitz, A. Sigal, M. Milyavsky, I. Zurer, G. Shohat, N. Goldfinger, and V. Rotter Change of the death pathway in senescent human fibroblasts in response to DNA damage is caused by an inability to stabilize p53 Mol. Cell. Biol. 21 2001 1552 1564
86. S.P. Cregan, J.G. MacLaurin, C.G. Craig, G.S. Robertson, D.W. Nicholson, D.S. Park, and R.S. Slack Bax-dependent caspase-3 activation is a key determinant in p53-induced apoptosis in neurons J. Neurosci. 19 1999 7860 7869
87. H. Xiang, Y. Kinoshita, C.M. Knudson, S.J. Korsmeyer, P.A. Schwartzkroin, and R.S. Morrison Bax involvement in p53-mediated neuronal cell death J. Neurosci. 18 1998 1363 1373
88. D. Uberti, M. Belloni, M. Grilli, P. Spano, and M. Memo Induction of tumour-suppressor phosphoprotein p53 in the apoptosis of cultured rat cerebellar neurones triggered by excitatory amino acids Eur. J. Neurosci. 10 1998 246 254
89. C. Culmsee, and M.P. Mattson p53 in neuronal apoptosis Biochem. Biophys. Res. Commun. 331 2005 761 777
90. C. Culmsee, X. Zhu, Q.S. Yu, S.L. Chan, S. Camandola, Z. Guo, N.H. Greig, and M.P. Mattson A synthetic inhibitor of p53 protects neurons against death induced by ischemic and excitotoxic insults, and amyloid β-peptide J. Neurochem. 77 2001 220 228
91. C. Culmsee, J. Siewe, V. Junker, M. Retiounskaia, S. Schwarz, S. Camandola, S. El-Metainy, H. Behnke, M.P. Mattson, and J. Krieglstein Reciprocal inhibition of p53 and nuclear factor-κB transcriptional activities determines cell survival or death in neurons J. Neurosci. 23 2003 8586 8595
92. X. Zhu, Q.S. Yu, R.G. Cutler, C.W. Culmsee, H.W. Holloway, D.K. Lahiri, M.P. Mattson, and N.H. Greig Novel p53 inactivators with neuroprotective action: syntheses and pharmacological evaluation of 2-imino-2,3,4,5,6,7- hexahydrobenzothiazole and 2-imino-2,3,4,5,6,7-hexahydrobenzoxazole derivatives J. Med. Chem. 45 2002 5090 5097
93. E. Tamagno, M. Parola, M. Guglielmotto, G. Santoro, P. Bardini, L. Marra, M. Tabaton, and O. Danni Multiple signaling events in amyloid β-induced, oxidative stress-dependent neuronal apoptosis Free Radic. Biol. Med. 35 2003 45 58
94. L. Gasparini, M. Racchi, G. Binetti, M. Trabucchi, S.B. Solerte, D. Alkon, R. Etcheberrigaray, G. Gibson, J. Blass, R. Paoletti, and S. Govoni Peripheral markers in testing pathophysiological hypotheses and diagnosing Alzheimer's disease FASEB J. 12 1998 17 34
95. M. Racchi, and S. Govoni Rationalizing a pharmacological intervention on the amyloid precursor protein metabolism Trends Pharmacol. Sci. 20 1999 418 423
96. D.A. Butterfield, T. Reed, S.F. Newman, and R. Sultana Roles of amyloid β-peptide-associated oxidative stress and brain protein modifications in the pathogenesis of Alzheimer's disease and mild cognitive impairment Free Radic. Biol. Med. 43 2007 658 677
97. D.A. Butterfield, and D. Boyd-Kimball The critical role of methionine 35 in Alzheimer's amyloid β-peptide (1-42)-induced oxidative stress and neurotoxicity Biochim. Biophys. Acta 1703 2005 149 156
98. D.A. Butterfield, S. Griffin, G. Munch, and G.M. Pasinetti Amyloid β-peptide and amyloid pathology are central to the oxidative stress and inflammatory cascades under which Alzheimer's disease brain exists J. Alzheimers Dis. 4 2002 193 201
99. E. Tamagno, M. Parola, P. Bardini, A. Piccini, R. Borghi, M. Guglielmotto, G. Santoro, A. Davit, O. Danni, M.A. Smith, G. Perry, and M. Tabaton β-site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways J. Neurochem. 92 2005 628 636
100. F. Murray-Zmijewski, E.A. Slee, and X. Lu A complex barcode underlies the heterogeneous response of p53 to stress Nat. Rev. Mol. Cell Biol. 9 2008 702 712
101. S. Di Giovanni, C.D. Knights, M. Rao, A. Yakovlev, J. Beers, J. Catania, M.L. Avantaggiati, and A.I. Faden The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration EMBO J. 25 2006 4084 4096
102. A. Tedeschi, and S. Di Giovanni The non-apoptotic role of p53 in neuronal biology: enlightening the dark side of the moon EMBO Rep. 10 2009 576 583
103. A. Tedeschi, T. Nguyen, R. Puttagunta, P. Gaub, and S. Di Giovanni A p53-CBP/p300 transcription module is required for GAP-43 expression, axon outgrowth, and regeneration Cell Death Differ. 16 2009 543 554
104. C. Lanni, D. Uberti, M. Racchi, S. Govoni, and M. Memo Unfolded p53: a potential biomarker for Alzheimer's disease J. Alzheimers Dis. 12 2007 93 99
105. C. Lanni, M. Racchi, S. Stanga, G. Mazzini, A. Ranzenigo, R. Polotti, M. Memo, S. Govoni, and D. Uberti Unfolded blood p53 as predictive signature from mild cognitive impairment to Alzheimer's disease J. Alzheimers Dis. 20 2010 97 104
106. X. Zhou, and J. Jia P53-mediated G(1)/S checkpoint dysfunction in lymphocytes from Alzheimer's disease patients Neurosci. Lett. 468 2010 320 325
107. J. Serrano, A.P. Fernández, R. Martínez-Murillo, and A. Martínez High sensitivity to carcinogens in the brain of a mouse model of Alzheimer's disease Oncogene 29 2010 2165 2171
108. D. Uberti, G. Cenini, L. Olivari, G. Ferrari-Toninelli, E. Porrello, C. Cecchi, A. Pensalfini, G. Liguri, S. Govoni, M. Racchi, and M. Maurizio Over-expression of amyloid precursor protein in HEK cells alters p53 conformational state and protects against doxorubicin J. Neurochem. 103 2007 322 333
109. G. Cenini, G. Maccarinelli, C. Lanni, S.A. Bonini, G. Ferrari-Toninelli, S. Govoni, M. Racchi, D.A. Butterfield, M. Memo, and D. Uberti Wild type but not mutant APP is involved in protective adaptive responses against oxidants Amino Acids 39 2010 271 283
110. C. Lanni, L. Nardinocchi, R. Puca, S. Stanga, D. Uberti, M. Memo, S. Govoni, G. D'Orazi, and M. Racchi Homeodomain interacting protein kinase 2: a target for Alzheimer's β amyloid leading to misfolded p53 and inappropriate cell survival PLoS One 5 2010 e10171
111. S. Stanga, C. Lanni, S. Govoni, D. Uberti, G. D'Orazi, and M. Racchi Unfolded p53 in the pathogenesis of Alzheimer's disease: is HIPK2 the link? Aging (Albany NY) 2 2010 545 554
112. F.D. Miller, C.D. Pozniak, and G.S. Walsh Neuronal life and death: an essential role for the p53 family Cell Death Differ. 7 2000 880 888
113. S.M. de la Monte, Y.K. Sohn, and J.R. Wands Correlates of p53 and Fas (CD95)-mediated apoptosis in Alzheimer's disease J. Neurol. Sci. 152 1997 73 83
114. Y. Kitamura, S. Shimohama, W. Kamoshima, Y. Matsuoka, Y. Nomura, and T. Taniguchi Changes of p53 in the brains of patients with Alzheimer's disease Biochem. Biophys. Res. Commun. 232 1997 418 421
115. R. Seidl, S. Fang-Kircher, B. Bidmon, N. Cairns, and G. Lubec Apoptosis-associated proteins p53 and APO-1/Fas (CD95) in brains of adult patients with Down syndrome Neurosci. Lett. 260 1999 9 12
116. C. Lanni, M. Racchi, G. Mazzini, A. Ranzenigo, R. Polotti, E. Sinforiani, L. Olivari, M. Barcikowska, M. Styczynska, J. Kuznicki, A. Szybinska, S. Govoni, M. Memo, and D. Uberti Conformationally altered p53: a novel Alzheimer's disease marker? Mol. Psychiatry 13 2008 641 647
117. D. Uberti, G. Cenini, S.A. Bonini, M. Barcikowska, M. Styczynska, A. Szybinska, and M. Memo Increased CD44 gene expression in lymphocytes derived from Alzheimer disease patients Neurodegener. Dis. 7 2010 143 147
118. N.M. Tassabehji, J.W. VanLandingham, and C.W. Levenson Copper alters the conformation and transcriptional activity of the tumor suppressor protein p53 in human Hep G2 cells Exp. Biol. Med. (Maywood) 230 2005 699 708
119. G. Perry, X. Zhu, and M.A. Smith Do neurons have a choice in death? Am. J. Pathol. 158 2001 1 2
120. X. Zhu, A.K. Raina, G. Perry, and M.A. Smith Alzheimer's disease: the two hit hypothesis Lancet Neurol. 3 2004 219 226
121. A.G. Wiese, R.E. Pacifici, and K.J. Davies Transient adaptation of oxidative stress in mammalian cells Arch. Biochem. Biophys. 318 1995 231 240
122. A. Nunomura, R.J. Castellani, X. Zhu, P.I. Moreira, G. Perry, and M.A. Smith Involvement of oxidative stress in Alzheimer disease J. Neuropathol. Exp. Neurol. 65 2006 631 641
123. S. Ueda, H. Masutani, H. Nakamura, T. Tanaka, M. Ueno, and J. Yodoi Redox control of cell death Antioxid. Redox Signal. 4 2002 405 414
124. J. Buzek, L. Latonen, S. Kurki, K. Peltonen, and M. Laiho Redox state of tumor suppressor p53 regulates its sequence-specific DNA binding in DNA-damaged cells by cysteine 277 Nucleic Acids Res. 30 2002 2340 2348